Additional protein intake limits weight regain after weight loss in humans
British Journal of Nutrition (2005), 93, 281–289
Additional protein intake limits weight regain after weight loss in humans
Manuela P. G. M. Lejeune*, Eva M. R. Kovacs and Margriet S. Westerterp-Plantenga
Department of Human Biology, Maastricht University, P.O. Box 616, 6200 MD Maastricht, The Netherlands
(Received 28 January 2004 – Revised 7 July 2004 – Accepted 21 September 2004)
Since long-term weight maintenance (WM) is a major problem, interventions to improve WM are needed. The aim of the study was toinvestigate whether the addition of protein to the diet might limit weight regain after a weight loss of 5 – 10 % in overweight subjects. In arandomised parallel study design, 113 overweight subjects (BMI 29·3 (SD 2·5) kg/m2); age 45·1 (SD 10·4) years) followed a very-low-energy diet for 4 weeks, after which there was a 6-month period of WM. During WM, subjects were randomised into either a proteingroup or a control group. The protein group received 30 g/d protein in addition to their own usual diet. During the very-low-energydiet, no differences were observed between the groups. During WM, the protein group showed a higher protein intake (18 % v. 15 %;P, 0·05), a lower weight regain (0·8 v. 3·0 kg; P, 0·05), a decreased waist circumference (2 1·2 (SD 0·7) v. 0·5 (SD 0·5 ) cm; P, 0·05)and a smaller increase in respiratory quotient (0·03 (SD 0·01) v. 0·07 0·01; (SD/)P , 0·05) compared with the control group. Weightregain in the protein group consisted of only fat-free mass, whereas the control group gained fat mass as well. Satiety in the fastedstate before breakfast increased significantly more in the protein group than in the control group. After 6 months follow-up, bodyweight showed a significant group £ time interaction. A protein intake of 18 % compared with 15 % resulted in improved WM in over-weight subjects after a weight loss of 7·5 %. This improved WM implied several factors, i.e. improved body composition, fat distribution,substrate oxidation and satiety.
Substrate oxidation: Weight maintenance: Body composition: High protein
A common treatment for obesity is weight reduction.
than is expected from its energy content alone (Anderson
Although short-term weight loss programmes have proved
1994). Several studies have shown that a high-protein
to be successful, long-term weight maintenance (WM) is a
lunch decreases later food intake more than a lunch low
major problem (Kramer et al. 1989; Wadden et al. 1994;
in protein (Booth et al. 1970; Barkeling et al. 1990;
Pasman et al. 1997a,b; Westerterp-Plantenga et al. 1998).
Latner & Schwartz, 1999). Westerterp-Plantenga et al.
Successful weight maintenance is of importance for lowering
(1999) showed an increased satiety effect of a high-protein
risk factors for cardiovascular and other diseases (Goldstein,
diet despite similar energy intake. Finally, protein has also
1992; Wing et al. 1992; Van Gaal et al. 1997). To improve the
been shown to have low energy efficiency during overfeed-
metabolic profile, it is not necessary to achieve the ideal body
ing (Dulloo & Jacquet, 1999; Stock, 1999), a situation that
weight: a weight reduction of 5 – 10 % is often sufficient to
is comparable to a weight regain situation. Although the
induce a clinically relevant effect (Goldstein, 1992). To pre-
effect of dietary protein has been examined in weight-
serve these beneficial effects of weight reduction, an
loss studies (Skov et al. 1999; Dumesnil et al. 2001;
improvement in long-term WM is necessary.
Layman et al. 2003), the effect of additional protein
Pasman et al. (1999) showed that weight regain was
intake on WM has not yet been studied. The aim of this
slower when the body composition of the weight regained
study was to investigate whether the addition of protein
consisted of a greater fat-free mass (FFM) due to physical
to the diet might limit weight regain after a weight loss
activity. We hypothesise that weight regain may be limited
of 5 – 10 % in moderately overweight subjects.
if the inevitable increase in body weight consists of a largerFFM, for instance achieved by the consumption of anappropriate substrate. For this, we suggest an increased
protein intake, because of its potential to increase FFM
(Jean et al. 2001). Furthermore, it is known that, of allthe macronutrients, protein seems to be the most satiating.
One hundred and forty moderately overweight male and
Protein consumption suppresses short-term food intake
female subjects (BMI 25 – 35 kg/m2, age 18 – 60 years)
more than that of fats or carbohydrates, and even more
were recruited for this study by advertisements in local
Abbreviations: FFM, fat-free mass; FM, fat mass; PAL, physical activity level; REE, resting energy expenditure; RQ, respiratory quotient; TBW, total body
water; TEE, total energy expenditure; TFEQ, Three Factor Eating Questionnaire; VLED, very-low-energy diet; WM, weight maintenance.
* Corresponding author: Ms M. P. G. M. Lejeune, fax þ 31 43 367 09 76, email M.Lejeune@HB.Unimaas.NL
BMI was calculated as body weight divided by height2
All the subjects were in good health, were non-smokers,
were not using medication and were at most moderate alco-
Waist:hip ratio. The distribution of fat was investigated
hol users. A written informed consent was obtained from
by measuring the waist and hip circumferences, and then
all the participants. The Medical Ethics Committee of the
calculating the waist:hip ratio. The waist circumference
Academic Hospital in Maastricht approved the study.
was measured at the site of the smallest circumference
Twenty subjects did not start the study due to relocation,
between the rib cage and the iliac crest, with the subjects
a change of job or an inability to fulfil the schedule with
standing. The hip circumference was measured at the site
visits to the university. Intention-to-treat applied for 120
of the largest circumference between the waist and the
subjects. During the first week, seven subjects dropped
thighs. The waist:hip ratio was calculated by dividing the
out because of difficulty maintaining the very-low-energy
waist circumference by the hip circumference.
diet (VLED). They had been meant to participate in the
Body composition. Total body water (TBW) was
additional-protein group. Their baseline characteristics
measured using the 2H2O dilution technique (Schoeller
did not affect the averages of the baseline measurements
et al. 1980; Van Marken Lichtenbelt et al. 1994). In the
of the treatment group. Thus, 113 subjects completed the
evening, the subjects collected a background urine
study. Subject characteristics are shown in
sample and then ingested a dose of 2H-enriched water(2H2O), after which they refrained from consuming fluidand food. The following morning, a urine sample from
the second voiding was collected between 08.00 h and
After the subjects’ baseline characteristics had been deter-
10.00 h. The concentration of 2H in the urine samples
mined, they were divided into two similar groups, stratified
was measured using an isotope ratio mass spectrometer
for gender, BMI, age, eating behaviour (Three Factor
(Micromass Optima, Manchester, UK). TBW was obtained
Eating Questionnaire (TFEQ); Stunkard & Messick,
by dividing the measured 2H dilution space by 1·04
1985; Westerterp-Plantenga et al. 1999) and resting
(Schoeller et al. 1980). FFM was calculated by dividing
energy expenditure (REE). Both groups followed a
the TBW by the constant hydration factor 0·73, which
VLED intervention for 4 weeks in order to initiate
can be used for adult subjects (Schoeller, 1996). The
weight loss. After this weight loss period, a WM period
weight loss and weight maintenance periods were long
of 6 months followed. Subjects in both groups visited the
enough to establish a stable hydration of FFM. Fat mass
university six times. During these visits, the measurements
(FM) was calculated by subtracting FFM from body
were carried out as described in the Measurements section
weight. FM expressed as a percentage of total body mass
below. Moreover, the subjects were asked by a dietitian
how they felt, how they considered taking part in the
Attitude towards eating. To determine whether attitude
study and whether they had any specific questions. Further-
towards food intake changed during the experiment, a
more, dietary counselling was provided upon request for all
Dutch translation of the TFEQ was used (Stunkard & Mes-
sick, 1985; Westerterp-Plantenga et al. 1999). The first
One of the groups was provided with additional protein
factor of the TFEQ (F1) measures cognitive restrained
(protein group, n 53), while the other group did not receive
eating: control of food intake by thought and will-power.
this additional protein (control group, n 60). Since, similar
The second factor (F2) represents disinhibition: an inciden-
to previous meal-replacement studies (Ditschuneit et al.
tal inability to resist eating cues, or inhibition of dietary
1999; Flechtner-Mors et al. 2000; Rothacker 2000;
restraint, and emotional eating. The third factor (F3) exam-
Ashley et al. 2001; Allison et al. 2003), no placebo was
ines the subjective feeling of general hunger.
used for this control group, we included repeated measure-
In addition, the Herman – Polivy questionnaire was used
ments of dietary restraint to check whether additional diet-
to determine the frequency of dieting (Herman & Polivy,
differently. After 6 months of WM, the additional protein
Post-absorptive appetite profile. To determine the post-
intake was stopped. Six months after WM, all the subjects
absorptive appetite profile, hunger and satiety were rated
were asked to return to the university for a follow-up
on anchored 100 mm visual analogue scales in the morning
measurement of body weight. For this measurement,
thirty-one subjects in the protein group and thirty-nine sub-
Blood parameters. A fasting blood sample of 10 ml was
jects in the control group returned.
taken and mixed with EDTA to prevent clotting. Plasmawas obtained by centrifugation (at 3000 U/min for 10 minat 48C), frozen in liquid nitrogen and stored at 2 808C
until further analysis. Plasma glucose concentrations were
The following measurements were executed to determine
determined using the hexokinase method (Glucose HK
125 kit; ABX diagnostics, Montpellier, France). The
Body weight and BMI. Body weight was measured on a
Wako NEFA C-kit (Wako Chemicals, Neuss, Germany)
digital balance (model 707, Seca, Hamburg, Germany;
was used to determine free fatty acid concentrations. Insu-
weighing accuracy of 0·1 kg) with subjects in their under-
lin concentrations were measured using the RIA-kit (Insu-
wear, in a fasted state and after voiding their bladder.
lin RIA-100; Kabi-Pharmacia, Uppsala, Sweden). The
Height was measured using a wall-mounted stadiometer
glycerol kinase method was used to determine glycerol
(model 220, Seca, Hamburg, Germany).
concentrations (Boehringer Mannheim GmbH, Mannheim,
Additional protein intake and weight maintenance
Germany). Triacylglycerol was measured using the GPO-
& Webster, 1977) was taken for the usual energy storage
trinder kit (Sigma Diagnostics Inc., St Louis, MO, USA).
of FM and FFM (A). If body weight gain consisted of
The b-hydroxybutyrate dehydrogenase method (Sigma
only FFM while FM decreased, 52 MJ/kg FFM gain
Diagnostics Inc., St Louis, MO, USA) was used to deter-
(Pullar & Webster, 1977) and 30 MJ/kg FM loss were
mine b-hydroxybutyrate concentration. Leptin concen-
trations were measured using the human leptin RIA-kit
ES (MJ/d) ¼ (D body weight (kg) £ 30)/number
(Linco Research Inc., St Charles, MO, USA).
Adverse events. Adverse events during treatment were
ES (MJ/d)¼ ((DFFM (kg) £ 52) 2 (DFM (kg) £ 30))/
recorded and the severity and outcome specified.
REE and substrate oxidation. In a random subset of
To see whether a higher percentage of energy ingested as
subjects (n 75), REE and substrate oxidation were
protein in the diet could lower the energy efficiency,
measured by means of an open-circuit ventilated hood
which is known already as the ‘Stock’ hypothesis
system. REE was measured in the morning with subjects
(Dulloo & Jacquet, 1999; Stock, 1999), we used the fol-
in a fasted state while lying supine for 30 min. Gas ana-
lowing equation to calculate energy efficiency (Eeff):
lyses were performed by a paramagnetic oxygen analyser(type 500A, Servomex, Crowborough, Sussex, UK) and
Eeff ðkg=MJÞ ¼ body weight regain ðkgÞ=ðEI ðMJ=dÞ
an IR carbon dioxide analyser (type 500A, Servomex,
Crowborough, Sussex, UK), similar to the analysissystem described by Schoffelen et al. (1997). Calculation
of REE was based upon the Weir’s formulas (Weir,1949). Respiratory quotient (RQ) was calculated as CO2
The VLED provided 2·1 MJ/d (carbohydrate – protein – fat
42:44:14 energy percentage) (Modifast, Novartis Nutrition,
Physical activity. The same subset of subjects who
Breda, The Netherlands) and was supplied in three sachets
underwent metabolic testing was used to measure physical
daily that were dissolved in water to obtain a milk shake,
activity level (PAL). PAL was determined using a uniaxial
pudding, soup or muesli. Vegetables and fruit were allowed
accelerometer (CSA, CSAB, Inc. Stamford, CT, USA.)
in addition to Modifast. The aim was a body weight loss of
(Ekelund et al. 2000), or a tri-axial accelerometer for
movement registration (Tracmor Maastricht University,Maastricht, The Netherlands.) (Goris et al. 2001), during
1 week. Subjects wore the CSA or Tracmor duringwaking hours on a belt at waist level on their back. The
After the VLED period, the WM period started, in which
different accelerometers were randomised over the two
all subjects were allowed to eat their habitual diet again.
groups. Half the subjects in the protein group and the con-
During the WM phase, the subjects in the protein group
trol group received the CSA, the other half received the
received 30 g additional protein per day. This was provided
Tracmor. Subjects received the same accelerometer every
as a sachet of pure protein (protein source calcium casei-
nate, 1·4 % calcium) per day to be dissolved in water,
PAL was calculated using the following equations:
giving rise to a vanilla-flavoured drink. The protein drinkcontained no carbohydrate or fat. Subjects were required
to consume the protein drink at lunch or in the afternoon.
¼ ð0·000001379 £ ðcounts=day £ 5ÞÞ þ 1·113
In this way, we aimed at an energy intake comprising18 – 20 % protein/d, depending on the subject’s usual
¼ 21·259 þ ð1·552 £ REEÞ þ ð0·076 £ counts=minÞ
Data are presented as mean and standard deviation (SD).
in which TEE is total energy expenditure (MJ/d) and REE
A two-factor repeated measures ANOVA was carried out
is resting energy expenditure (MJ/d).
to determine possible differences between the protein and
Protein intake. Compliance with additional protein
control groups in all measured parameters over time.
intake was checked by taking 24 h urine samples after 3
When appropriate, a factorial ANOVA was used for analys-
months WM and analysing these for nitrogen. Energy
ing differences between the two groups. Post hoc analyses
intake from protein was calculated from the 24 h nitrogen
were made with the Scheffe F-test. A P value , 0·05 was
output according to the formula of Isaksson (1980):
regarded as statistically significant. Statistical procedures
were performed using Statview SE þ Graphics (AbacusConcepts, Berkeley, CA, USA).
¼ ðnitrogen output in 24 h urine ðg=dÞ þ 2 gÞ £ 6·25
Energy intake and energy efficiency. Energy intake wascalculated as TEE plus energy storage (ES). Energy storage
The effects did not differ between men and women so data
was calculated from the composition of the energy stored.
from both genders were analysed together. No adverse
A figure of 30 MJ per kilogram body weight gain (Pullar
events occurred. Subjects continuously reported that they
Additional protein intake and weight maintenance
felt positive about taking part in the study. They confirmed
that ample attention was given to their questions.
During the VLED period, the changes described belowoccurred, which did not differ between the subsequent pro-
tein and control groups Subjects lost a significant
of their original body weight (P, 0·0001). The mean change
in body weight for both groups over time is shown in
This consisted of 4·0 (SD 1·7) kg FM and 2·3 (SD 1·7) kg
FFM. Waist circumference was also significantly reducedover time. Attitude towards eating showed some significant
changes over time Cognitive restraint (F 1, TFEQ)increased significantly; disinhibition (F 2, TFEQ) and gen-
eral hunger scores (F 3, TFEQ) decreased during weight
loss REE and RQ decreased during weight loss
TEE decreased in both groups, but this only
reached significance in the control group. Fasting blood glu-
cose, insulin, triacylglycerol and leptin levels showed a sig-
nificant decrease with weight loss, and b-hydroxybutyrate,
glycerol and free fatty acids showed a significant increase
Compliance with the additional protein was shown by a
higher amount of nitrogen in 24 h urine in the protein
group compared with the control group (14·3 (
v. 11·2 (SD 3·5) g/d; P, 0·05). The protein intake in the
protein group was 101·7 (SD 22·2) g/d, which was signifi-
cantly higher than the 82·7 (SD 22·0) g/d in the control
group (P, 0·05). When expressed as percentage of
energy intake from protein, significant differences per-
sisted, with 18 % in the protein group and 15 % in the
During WM, percentage body weight regain, as well as
rate of regain, was significantly lower in the protein
group than the control group The netpercentage body mass lost after the WM period compared
Fig. 1. The change in body weight over time for the protein group
(X) (n 53) and the control group (W) (n 60). Values are means with
standard deviations of the mean shown by vertical bars.
Table 3. Fasting blood-parameters of the protein (n 32) and the control (n 43) group at baseline, after 4 weeks on a very-low-energy diet(VLED; Modifast) and after 3 months weight maintenance
* P, 0·05 compared with baseline (repeated measures ANOVA).
† P, 0·05 compared with control group (factorial ANOVA).
‡ P, 0·05 interaction treatment £ time (two-factor repeated measures ANOVA).
with baseline was significantly higher in the protein group
REE returned to almost baseline values in both groups
than the control group (6·7 (SD 7·2) % v. 3·8 (SD 4·8) %;
during WM To assess possible differences in
P, 0·05). The protein group showed a decrease in waist
REE adjusted for FFM between groups, we analysed the
circumference during WM, whereas the control group
residuals of the regression of REE v. FFM. The residual
showed an increase (2 1·2 (SD 0·7) cm v. 0·5 (SD 0·5)
analysis showed no significant group £ time interaction.
cm; P, 0·05). FFM stayed significantly lower during
The increase in RQ during WM was significantly smaller
WM compared with baseline in both groups. FM in theprotein group continued to decrease during WM, whileFM increased in the control group (2 0·9 (SD 0·7) kg v.
1·7 (SD 0·4) kg; P, 0·005) Cognitive restraintscores stayed significantly higher during WM comparedwith baseline in both groups. No differences were seen inthe change in cognitive restraint during the study betweenthe groups. Disinhibition stayed significantly lower inboth groups, and general hunger decreased in bothgroups. Satiety in the fasted state before breakfastincreased significantly during WM in the protein groupbut not in the control group The increasein satiety was significantly higher in the protein groupthan the control group. The hunger scores in the fastedstate before breakfast did not change over time ineither group.
Fig. 3. The changes in body weight (B), fat-free mass (B) and fat
Fig. 2. The weight regain during weight maintenance (expressed as
mass (A) for (a) the protein group (n 53) and (b) the control group
percentage of the weight loss) for the protein (B) (n 53) and the
(n 60) during the study compared with baseline. Values are means
control (A) (n 60) groups. Values are means with standard deviations
with standard deviation of the mean shown by vertical bars. VLED,
of the mean shown by vertical bars. *P, 0·05 compared with control
change after the very-low-energy diet period; 3 months WM,
group, †P, 0·05 compared with 1 month weight maintenance,
change after 3 months weight maintenance; 6 months WM, change
‡P, 0·05 compared with 2 months weight maintenance.
Additional protein intake and weight maintenance
in the protein group than the control group (0·03 (SD 0·01)
The composition of the body mass regained was
v. 0·07 (SD 0·01); P, 0·05), indicating a smaller decrease in
different for the protein and the control groups. The body
fat oxidation in the protein group than in the control group.
mass regained in the protein group consisted only
The increase in RQ was not related to weight regain
of FFM, whereas the FM still decreased during WM,
(P. 0·05). No changes in PAL were seen over time and
which resulted in a lower percentage of body fat. In the
between groups A trend for a lower energy effi-
control group, the composition of the body mass regain
ciency of the protein group than the control group was
was FM as well as FFM. The observation that body mass
found after 6 months WM (3·0 £ 1024 (SD 0·003) kg/MJ
regain consisting only of FFM results in a slower weight
v. 0·001 (SD 0·002) kg/MJ; P¼ 0·12).
regain is in line with our hypothesis that when the
Leptin concentrations stayed significantly lower after
composition of the weight regained consists of a greater
treatment compared with baseline in the protein group
FFM, the inevitable increase in body mass will be
Glucose concentrations stayed significantly
slower. Here, however, we have shown that this was due
lower after treatment compared with baseline in the control
to increased protein intake without a change in physical
group. Insulin concentrations stayed significantly lower
activity, whereas in the study of Pasman et al. (1999),
after treatment compared with baseline in both groups.
the cause appeared to be increased physical activity.
b-Hydroxybutyrate, glycerol and free fatty acid concen-
In addition to a beneficial effect of dietary protein during
trations returned almost to baseline values during weight
weight loss (Skov et al. 1999; Astrup, 2001; Dumesnil et al.
regain Triacylglycerol concentrations during
2001; Layman et al. 2003), protein also appears to support
WM were significantly lower in the protein group than
Although subjects were asked to consume 30 g/d protein
The change in body weight of the subset of subjects
in addition to their usual diet, the analysis of the results
(protein n 31, control n 39) who were also measured
showed a mean difference of 19 g/d between the protein
after 6 months follow-up is shown in The analysis
and the control group. This could imply that subjects
of the follow-up measurement of body weight showed a
in the protein group replaced part of their usual protein
significant group £ time interaction.
intake by the protein that was provided to them. Sincethis was a study under free-living conditions, the carbo-hydrate and fat content of the weight maintenance diet
With respect to satiety, we found a greater increase in post-
In the present study, we investigated whether the addition
absorptive satiety in the protein group during WM, although
of protein to the diet might limit weight regain after a
their energy intake did not differ significantly from that of the
weight loss of 5 – 10 % in moderately overweight men
control group. Short-term differences in digestion, absorp-
and women. The results show that subjects who consumed
tion and energy expenditure between different protein
18 % of their energy intake as protein regained less weight
sources have been shown (Boirie et al. 1997; Mikkelsen
during 6 months WM (0·8 kg), compared with subjects who
et al. 2000). Boirie et al. (1997) introduced the concept of
consumed 15 % of their energy intake as protein (3·0 kg).
‘fast’ and ‘slow’ proteins, based upon the differences in
This was independent of changes in cognitive restraint,
digestion and absorption of these proteins. These short-
physical activity, REE, TEE and hunger scores since
term effects may be related to increases in the concentrations
these parameters did not differ between groups.
of gut hormones, such as glucagon-like peptide-1 (Flint et al.
1998; Gutzwiller et al. 1999; Naslund et al. 1999) and chole-cystokinin (Schick et al. 1991; Burton-Freeman et al. 2002;Kissileff et al. 2003). However, this probably does not applyto post-absorptive satiety. Animal protein has been shown tointroduce a higher energy expenditure (Mikkelsen et al.
2000), and, in the longer term, the higher post-absorptivesatiety and thermogenesis were sustained with high-proteindiets consisting of a variety of proteins from different sources(Dulloo & Jacquet, 1999; Westerterp-Plantenga et al. 1999;Dumesnil et al. 2001; Westerterp-Plantenga et al. 2004).
Moreover, a relationship between satiety and thermogenesishas been shown (Crovetti et al. 1998; Westerterp-Plantengaet al. 1999) with using high-protein diets. We thereforesuggest that the higher post-absorptive satiety is due toincreased thermogenesis.
The observation that the increase in REE as a function of
Fig. 4. The change in body weight for the subjects with follow-up in
FFM during WM did not differ significantly might be due to
the protein group (B) (n 31) and the control group (A) (n 39) during
the lack of a significant difference in the increase of FFM.
the study compared with baseline. Values are means with standard
The slower increase in RQ in the protein group reflects a
deviations of the mean shown by vertical bars. *P, 0·05 compared
with the control group. VLED, change after the very-low-energy
Although the treatment with respect to number of visits,
diet period; WM 1, 2, 3, 6 change after 1, 2, 3 and 6 months weightmaintenance.
measurements and attention was identical in both groups,
there was no placebo used for the additional protein, simi-
lar to previous meal-replacement studies (Ditschuneit et al.
1999; Flechtner-Mors et al. 2000; Rothacker, 2000; Ashley
Allison DB, Gadbury G, Schwartz LG, Murugesan R, Kraker JL,
et al. 2001; Allison et al. 2003). The issue of the placebo is
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FIORENZO CONTI 1. PERSONAL HISTORY Department of Experimental & Clinical Medicine Section of Neuroscience & Cell Biology Università Politecnica delle Marche Via Tronto 10/A, Torrette di Ancona I-60020 Ancona (Italy) Phone 0039 071 220 6056 Faz email@example.com www.fiorenzocontigroup.it Birth Date and Place August 13, 1955 Villerupt (France) Current position