Circadian Monique
variation
Romon,
of diet-induced
Jean-Louis
Edme,
ABSTRACT The objective cadian variation ofdiet-induced favor weight gain among night time
snack.
1 700,
Nine
young
or 0100.
men
Energy
metabolic
rate.
ternoon the
time
than
when
sponse J
and
0.04)
=
higher
DIT
given
KEY
WORDS
ation,
shift
mean
measured
a meal
(P
is consumed
DIT
(P
=
0.06).
Diet-induced
the
snack. above
higher
0.002).
=
We
affects in the
at 0900,
by indirect
significantly
night DIT
must be considered 1993:57:476-80.
C/in Nutr
the same
was
was
and night
Jean-Louis
the
DIT basal
than
af-
re-
Am
circadian
vari-
work
ules requiring These workers
a rotation are used
hours that comprises Despite the fact that
shown gain
a20% of their daily energy intake (1-3). their 24-h energy intake is no different than
is different
ofthem suggest
depending
in the same in humans
practice: however a7.3 million on permanent shifts or on sched-
of morning, evening, and night work. to eating a snack during their working
that ofday workers, some on night work (4-7). Some studies indirectly of a diet
subjects
when
food
do tend
to gain
that
metabolic
on
the
the
that
there
was
available
time
weight
when
efficiency
it is eaten:
intake
intake
but
(4). Because
have
body
was a relative
a higher
only
Circadian for a long
it is much
its
changes stimuli ation
476
neither
This induced
and
ofdiet-induced
(8)
than
in EE (13,
variation. during
the
14). Only
two
of energy
metabolism
food
thermogenesis
intake
(to mimic
of day,
Some day studies
in the have
in response
of many
other
data on 24-h energy have been interested
investigators absence
nocturnal
shift
ie, between
Subjects
DIT.
workers’
whether thermogenesis of the usual 24-h energy
eating
morning,
patterns)
afternoon,
varied
and
with
time
night.
and methods
Subjects Nine young nonobese men participated volunteers. Data concerning some physical presented in Table 1. ofthe subjects had a history
have
studied
of thermogenic
examined
diurnal
to thermogenic Am J C/in Nuir
and they or subjects
were who
in the study characteristics
ofendocrine
not taking had traveled
as paid and
or metabolic
any drugs. Shift or night across time zones within
the previous six mo were excluded. All potential volunteers answered a questionnaire concerning their daily routine and sleep and meal schedule; those with irregular habits were excluded. Each selected subject pose ofthe experiment ticipate Helsinki
was informed before giving
The
study
consisted and
night.
of three
randomized
Between
each
was
eaten
at 0900
the afternoon
I
subject
From
with
the
during
session, the
snack
the
the Laboratoire
de Physiologic, 2 Supported
March
a time 22 and
5 wk.
within
morning the
session,
during same
for
During
night
the
three
during
session.
For
sessions:
it
and the Laboratoire Re-
gional Nord-Pas-de-Calais, and Davigel SA. 3 Address reprint requests to M Romon, Laboratoire de Medecine Travail, Facult#{233} de M#{233}decine,59045 Lille C#{233}dex, France.
du
vari-
1993:57:476-80.
Received
March
Accepted
for publication
Printed
25,
in USA.
CRE
I 700
Conseil
stimuli
INSERM,
at
the
de M#{233}decinedu Travail,
Lille, France. by grants from
morning, was
for 1 h preceding and 6 h after daily energy intake. This snack
at 0100
was
there
between
experiment
the
and
sessions:
session
conducted
each session EE was measured a snack representing 20% ofusual
each
in accordance in 1983.
design
span 5 d. The study June 6, 1988. All subjects completed
was
about the nature and purhis written consent to par-
and the study was conducted Declaration of 1975 as revised
afternoon,
has been known (10), yet despite
the rhythm
Numerous authors have collected (EE) (1 1 , 12) but few studies
circadian
nocturnal
of body weight, we propose the DIT, which could favor weight
less documented
studied
study was designed to investigate by a snack consisting of 20%
Experimental
weight
in the evening
variation of energy metabolism time in humans (9) and in animals
functions. expenditure in
evening
the regulation
(DIT) is relevant to the control hypothesis of a lower nocturnal gain.
this,
and
it was
as compared with availability in the morning. In a former study we found that among shift workers, those who gain the most weight do not differ with regard to their 24h energy
16). However. they failed to find a difference between morning and afternoon DIT, but morning and afternoon tests varied in duration ofthe postabsorptive state in the second study
disorders workers
eating is not a frequent work at night either
Frimat
( 1 5,
age are None
Introduction Night Americans
Paul
that
balance.
thermogenesis,
and
Afternoon
conclude
thermogenic
energy
Lescroart,
no. 86.80.33,
1992.
October
6. 1992.
© 1993 American
Society
for Clinical
Nutrition
Downloaded from www.ajcn.org by guest on July 13, 2011
was
were
and during the 6 h after 3 h of energy expenditure
Morning
(P
DIT
DIT
Boulenguez,
of this study was to assess a cirthermogenesis (DIT) that could workers used to eating a night
expenditure
calorimetry 1 h before was calculated as the
Charles
thermogenesis13
CIRCADIAN TABLE 1 Physical characteristics of the test meal*
VARIATION
OF
All gas-exchange of the nine subjects
and energy
content
ventilated cart with
Value
61.8 171 21.1 2274 544
± 2.31 ±
3.45
±
0.63
was
158
±
air was
drawn
inhaled
from
performed
through
with
the
canopy on both
with
a blower. air
the
between samples
air
0.65
were
air
of a
Horizon
in a plastic fastenings
canopy
flowing
use
the
into flow
so that
the
with
is provided
the air flowing through the system and passed mixing chamber for analysis. The rate of air
adjusted
Gas
± 37
system
expired
maintained
entering
and
the
stream;
mixing
chamber
was
0.85%.
analyzed
every
3 mm
and
an
automatic
calibration sequence was introduced every 20 mm, which introduced first compressed pure nitrogen into the analyzers to check for zero drift and second a calibration gas (20.0% 02, 0.75%
SE.
±
subject
mixed with the Horizon
were
the canopy
subject’s head was enclosed seal at the neck and velcro
Room
The
28 ± 2
measurements
hood;
(1 7). The a flexible
sides. Age (i) Weight (kg) Height (cm) Body massindext Meal (kJ) (kcal) *
477
DIT
t In kg/m2.
CO2. and the balance, At the was composed Dieppe,
offrozen
France).
identical
dishes
The
for all individuals;
derived
from
ofknown
relative
protein,
composition
composition the
fat, and
fractions
of total
carbohydrate EE under
was intake
0. 15, 0.35,
the same
Three
nental fee)
hours
breakfast
before
the
(bread,jam,
representing
20%
Experimental
butter,
of usual
metabolic
the
preceding
registered
For the 6 h before
For day
con-
and
had
the up in-
decaffeinated
and
eat
conditions and to Ferrannini
EE (kcal/min) In this
spent evening woken
0530
and
the
subjects
night
in the
to
arrived
he was
then
and night and had
each sat
test subjects arrived their standardized
of the three sessions quietly in the ward
ward;
they
allowed
to
in the ward meal 4 h be-
and after reading
was
a
and
V02
+ 1.10
were
used
VCO2
-
dioxide pressure,
to calculate
3.34
N
study
DIT
was
rate
measured
the energy
calculated
as is usually in quotation
as the
between
done marks
additional
0530
classically. For is used instead
EE had reached the resting as the 3-h EE and expressed
content
of the test
EE above
and
0600
instead
this reason of DIT.
the
value after 3 h, DIT as a percentage of
meal.
at
meal at home at 1800. At and his basal metabolic rate 0600:
urea nitrogen ( 18),
3.91
=
metabolic
Because the was calculated
breakfast.
afternoon the snack After subjects
dry (STPD) EE according
basal
test
there
temperature,
The volume ofoxygen consumed (V02) and carbon produced (VCO2) corrected to standard temperature
cof-
intake.
morning
session
volume,
a conti-
session subjects were instructed and to refrain from moderate
the
and
to have an was gently between
get to void
forehand. a meal,
energy
each diet
activity.
were instructed 05 1 5 the subject was
milk,
they
of the for
Calculations
protocol
physical
2200
snack
procedure
analyzers.
of the RMR, term “DIT”
For the day preceding not to change their usual heavy
morning
calibration
and
ditions at the different times of the day, subjects were given same meal 4 h before the night and afternoon snacks, made of frozen dishes (Davigel) representing 30% of usual energy take.
N2). at the beginning
and
breakfast or or watching
Statistics The results were conducted
are
expressed with the
as mean ± SE. Statistical statistical system (19).
of variance with use of a model for a single-factor with repeated measurements (GLM procedure, ment) was used to test whether between morning, afternoon, was
then
and
“DIT”
performed
experiment repeated state-
EE and DIT varied systematically and night. Contrast transformation
to evaluate
between
analyses Analysis
SAS
morning,
differences afternoon,
in premeal and
RMR
night.
television. After a 30-mm rest on a bed the resting metabolic was measured 1 h before the test snack. Afterward, 20 mm
outside
measured the
the canopy
continudusly
postprandial
EE
and examining the night.
slides
Gas-exchange
oxygen (Liston
beginning
measurements, for errors
and
the snack.
subjects to keep
them
void.
were awake,
lying even
Results
EE was During down
The and
premeal
night
was kept at 22-25 #{176}C. After gas-exchange was collected to determine urea nitrogen.
showed
Figure
a Horizon
Anaheim a Beckman
CA), OM-Il
were
made
metabolic
by open-circuit
measurement
cart
and an infrared optical Beckman) for carbon
system dioxide
medical analyzer measurements.
given
for
the
separately
no significant
effect
morning,
in Table oftime
afternoon, 2. Analysis
ofthe
day
1 shows patterns of EE after ingestion with premeal RMR, EE was significantly
the
=
there
which includes a turbine volume analyzer with a polarographic
in subjects
are
(P
first
0.02)
and
second
(P
hour
of
on RMR.
of the meal. higher dur0.003)
=
for
the
morning session. It was significantly higher during the first hour (P = 0.05) and lower during the fifth (P = 0.04) and sixth hours
(P
measurements
by using
analyzer Becker-2;
ing
RMR
sessions
variance
during
measurement
Indirect-calorimetry respirometry
for 6 h after
meal
Compared
Room temperature measurements, urine
(Sensormedics, transducer,
to eat the test
rate (RMR) subjects spent
0.006) was
during
the afternoon
no difference
session.
at any
time
During
with
the
the night premeal
Because EE was no higher and was in fact initial value after 3 h during all three sessions, culated Table snack,
as the 2 gives expressed
3-h
EE above the
“DIT”
as a percent
basal calculated ofthe
metabolic
lower “DIT”
than was
the cal-
rate.
during energy
session
level.
the
content
3 h after ofthe
the meal.
Downloaded from www.ajcn.org by guest on July 13, 2011
0.50, respectively. To measure the postsnack
snack
energy
were
complete
(Davigel,
of the
end
478
ROMON
TABLE 2 Premeal resting metabolic rate (RMR) and diet-induced (DIT) in nine subjects at different times of the day*
ET
AL
day, thermogenesis
“
and RMR
6.06
±
of meal)
15.9
± I .6tt
6.10 13.5
±
0.29
of meal)
±
l.8
(kJ/min)
of energy
content
RMR (kJ/min) of energy content
0.33
*
any
different
Significantly
from
different
afternoon
from
value.
night
value,
P
P
=
=
0.002,
0.04.
have §P
in the During
the morning
session
“DIT”
was significantly
session
(P
0.002).
Afternoon
“DIT”
tended
night “DIT” (P = Mean respiratory
0.06). quotient
session
during (P
± 0.02 ± 0.02
=
the
before
in the morning. 0.83 at night (NS). During
during the first hour after ± 0.03, and 0.86 ± 0.03 night sessions, respectively.
higher
meal
variation
the meal, which was 0.89 ± 0.02, (NS) for the morning, afternoon,
0.87 and
and
gastric
it was
study meal.
consumed.
to each
series
ifa
ofthe
be rejected
unpublished This result
three a
P
communication, differed from
not find any significant noon DIT. However.
24-h
emptying.
ofO.Ol,
was
authors insulin shown
during
which
function
is fitted
ofchange
rhythm
can
assumption
see Appendix
1992). that of Westrate
and
than
bolus
suggested dose
a more
by the
measured
fasting
evening
consisting ofdigestion mainly
involved important
regulates
the
rate
of nutrient
by Tai load
flux
et al (23), of nutrients
compared
rapid
gastric
to be slower
the
meavariation
changes
state
and
may
not
ofan and
reflect
obligatory processing
mediated
by the sym-
with
absorption
in digestion and abfactor is the rate of of nutrients
into
the
absorption.
This
ex-
who
a higher
found
was
six small
administered doses.
of nutrients
emptying after
a night
(24).
Gastric
meal
than
For
induced
response and enhanced nutrient storage. that morning gastric emptying is significantly
found
is
to explain
be due to circadian variation the thermic response to flu-
one.
the
an isoenergetic
after
be
(22).
which hence
DIT in the EE response
the extent
no circadian
state to the
ofprocesses known. One
planation
stage
cosine
values,
The
with
difference
on the circadian
quantitatively.
can then
a clear
Furthermore
ofthe
be assessed
showed
depending
system
and
not
of EE.
Circadian variation sorption is not well
a single present
fasting
a facultative
nervous
could
enough
be confounded
trients. It is an intricate mechanism component. which is the energy cost pathetic
a rhythm
0.633: see Appendix during the night DIT
however,
may
0.84
Discussion The
ofthe
ofnutrients,
other
(2 1 ). In fact, the premeal
the metabolic-rate
cases
than
± 0.02 in the afternoon, and 0.81 the three sessions it reached a peak
EE (20)
difficulty:
this
to be higher was
of
=
is not
Circadian variation of DIT might of the different factors underlying
ingestion
are
fail to
object that the use of a no meal is given, would
by an adaptation
duodenum
to the same
which
They
authors
period between
and
night
and
cir-
found. One might test. ie. a test when
in these
circadian
than
1% (20),
fed.
in resting
sessions,
the
0.04)
=
rhythm
the three
duration
and
a greater It has more
emptying after
as these been rapid
was
a morning
also meal
A (F. Halberg,
et al ( 16) who
did
difference between morning and afterin his study the subjects had a shorter
-
Morning
-
-
fasting
period
in the
so the
subjects
were
ditions.
afternoon not
tests
exactly
than
under
et al ( 1 5) compared
Capani
in the
the
same
oxygen
morning
tests
metabolic
con-
consumption
-
- .-
Night
-
after
the morning or evening meal with each meal being given after the same period offasting (I 2 h). He found a significantly higher oxygen consumption when the protein meal was given in the morning but no difference for the carbohydrate or fat meal. The response The
to a night circadian
observed of resting the this
meal
has
differences
can be explained EE and
not
variation
of the
factors
circadian
Circadian
variation
of resting
study
we chose
variation
we took
measure
EE should “DIT”
as the
test.
Because
as a reference
we were the same
we
involved
be discussed
metabolic rate although most EE above RMR measured
control
that variation
rhythmic
to nutrients.
a nonenergy
before. of response
factors:
response
above the basal DIT as additional
studied
pattern
by different
thermic
to
been
in the
in
first.
additional
studies premeal
In EE
calculated or during
interested
in circadian
metabolic
point
of the
50
0
1 Time
2 after
3 meal
4
5
6
(br)
FIG 1 . Patterns of energy expenditure after ingestion of a meal at different times ofthe day for a 60-mm period of measurement. . ± SE. Significantly different from premeal value: *J) < 0.05. P < 0.01.
Downloaded from www.ajcn.org by guest on July 13, 2011
afternoon
seen
are
for rhythm rejection it has been stated that
overcome
our
DIT
( I 3. 14).
subjects
(P
that we control
surements
0.06.
=
of feeding when
of circadian
by
Therefore,
true
observed in the overnight any significant difference
underestimated
± 2.2
et al (20).
phenomena:
EE. In humans it has been suggested of resting EE occur during the day
and
EE during
demonstrated A). However,
± 0.25
two
independent
evidence
be induced that
are
amplitude
difference nonenergy
t Significantly
:
find
Pullicino
account
of resting oscillations
they
little
resting
SE.
±
.
5.89 10.9
of meal)
that
very
as did
into
than a reduction we did not find
Night
Premeal RMR (kJ/min) DIT ( of energy content
rate,
takes
cadian variation that significant
Value Morning Premeal DIT (% Afternoon Premeal DIT (%
ie, basal
DIT”
CIRCADIAN (25),
but
have
to be confirmed
subjects
A blunted sistance
were
thermic
(26).
infusion,
Cauter that
they
ditions a nocturnal rise 50% for insulin secretion identical
meal
glucose ing
and
meal
of
relationship
secretion
and
the magnitude to a meal
times
evening.
by a night
of glucagon
on
difference
the
termines
liver
energy The
cost (33). facultative
by circadian
daily
cortisol an inverse
ofglucose in insulin
to be clarified.
counterregulatory
response
glucose
metabolism,
component
could of DIT
rhythmicity. protein
lead
also
substrate
cycling,
are under all ofthe
the influence of sympathetic control facultative response can be suppressed
receptor blockade (22). Among is modulated by true circadian
or sodium
catecholamines rhythmicity
the night importance
explain could, (26).
this
as the
study
evening
the phenomenon as in obesity, lead Other
A (36) scribed about
metabolic
and
suggested to eat.”
shift
is nocturnal to a reduced
as futile which
workers. utilization
years
ago,
Despite
these
of nutrients “more
response
work
to
resistance, which effect of glucose
as increased
hemoglobin
38)
have
been
facts
little
is known
and
as Halberg
is needed
on
de-
aspects
(in
German).
of the
V. Frimat
E, Burnond
chronobiology
18.
of nutrition:
20.
more
Chem Fed
J#{233}quier E. Twenty-four
hour
and resting metabolic rate in obese, moderately subjects. Am J Clin Nutr 1982:35:566-73.
Schutz
T, J#{233}quierE. Diet-induced
G.
Bessard
sured
over a whole
Nutr
I 984:40:542-52.
Apfelbaum
M,
day in obese
Reinberg
Bailey
D,
Johnson
A,
Capani
HRE.
of man
thermogenesis
and nonobese
Lacatis
D,
Kupprat
at rest. J AppI
F, Consoli
A, Del
Ferrannini
E. The
women.
Abulker
C,
I. Oscillations
Physiol
Ponte
theoretical
Pullicino
E, Goldberg
GR,
metabolism measured receiving cyclic and 199 1:80:57 1-82. 21.
Goldberg
and
mea-
Am J Clin Bostsarron
J,
in oxygen
con-
1973:34:467-70.
A, Ferrara
D, Guagnono
T, Sensi
basis
GR,
basal
Prentice
Elia
calorimetry:
statistics,
M. Energy
version
a review.
5 edition.
expenditure
and
by 24-h whole body calorimetry continuous parenteral nutrition. AM,
metabolic
ofindirect
rates
Davies
HL,
Murgatroyd
in men
and
women.
substrate
in patients Clin Sci
PR.
Eur
Cary.
Overnight
J Clin
Nutr
1988:42:137-44. 22.
23.
work on eating behavior of et travail. Paris: Masson,
Y,
in a 1 (in
energy expenditure obese, and control
Metabolism I 988:37:287-301. 19. SAS Institute Inc. SAS user’s guide: NC: SAS Institute Inc. 1985.
when 13
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(8)
We thank Franz Halberg for his helpful criticisms, suggestions, and calculations in Appendix A. We thank Bernadette Hennache for the urea nitrogen assay.
1. Debry G, Bleyer R. Influence of shift workers. In: Debry G, ed. Alimentation 1972:153-72 (in French).
1984:38:30-5 C, Demarcq-Leignel
Riou F. Circadian rhythm ofoxygen consumption and of respiratory quotient ofyoung adult women with spontaneous food intake and after energy restriction. Rev Eur Etud Clin Biol 197 I : I 6: 1 35-43 (in French).
15.
is parare higher
hypotheses
Wissenschatt M, Declercq
F. Some
sumption
is of physio-
of the
(37,
13.
14.
because almost by 3-adrenegic
only epinephrine (34), with a trough
insulin thermic
such
in
such
thermogenic
concentrations
nocturnal a few
that One
disturbances
triglyceride
among the
shows
progresses.
a de-
pumping,
(35). Whether this phenomenon remains to be demonstrated.
In conclusion, declines
12.
be modulated
occurring at 0320. Epinephrine-induced thermogenesis tially inhibited by basal insulin concentrations, which during logical
(32), which
Halberg
1 1. Ravussin
vs the
to a difference
mechanisms
turnover,
subshown insulin
the effect
insulin,
may
It includes
and how-
is unclear
and
Z Arbeit
work is needed on “when to eat.” J Nutr 1989:1 19:333-43. 9. Benedict FG. Factors affecting basal metabolism. J Biol I915:20:263-95. 10. AschoffJ, Pohl H. Rhytmic variations in energy metabolism. Proc I 970:29:1541-52.
hormones
Although
to glucose
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8.
to eve-
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Romon-Rousseaux
Furon D. Survey of eating behavior glass factory in Pas-de-Calais. Arch French).
response
been done in night-fasting the day and it has been between glucagon and in the
shift 7.
insulin
(29). Glucagon variation (30);
is eaten
AS, Wahlquist MC. Effect of shiftwork on canteen food purchase. J Occup Med l985;27:552-4. 4. Romon M, Beuscart R, Frimat P. Debry G, Furon D. Energy intake and weight gain according to rotation schedules in shift workers. Rev Epidemiol Sante Publique 1986:34:324-31 (in French). 5. Rutenfranz J, Colquhoun WP, Knauth P. Ghata JM. Biomedical and psychosocial aspects ofshiftwork. A review. Scand J Work Environ Health 1977:3:165-82. 6. Cervinka R, Kundi M, Koller M, Arnhog J. Eating behavior and
Moreover,
of a morning
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and
(28).
increase
meal molar
a higher to a mornbe mod-
magnitude
meal
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found could
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when
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the patterns have
ever, most circadian studies have jects who ate their meals during (3 1 ) that internal time relations differ
the
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between
in
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ofmorning
ning decrease growth hormone
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a constant
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nocturnal
plasma
and
be due
using
tolerance
ulated by counterregulatory concentration displays a clear temporal
night,
17% for plasma glucose and almost (28). More recently, when giving an
response
The
also
demonstrated
at different
insulin
(29).
could
a minimum study
the
state.
et al (27),
glucose
reaching
In a subsequent
during
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Van
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vs night
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presnack neglected
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for a first
morning
and
approximation
cosinor a cosine
analysis, function
which is based of the form f(t)
=
least-squared
a
three using
regression
of
M + A#{149}cos(wt + 0)
where
flt) is the
cients; halfthe
M is the mean level, termed mesor: A is the amplitude, range ofoscillation: w the angular frequency, 360/r where
r is the
period
value
on
af-
and
at time
so that
of the
function
360#{176} represents
regression
one
complete
coeffi-
cycle.
in
our case 24 h: and 0 is the time of the maximum, termed the acrophase (for each individual subject). For thermogenesis. the zero-amplitude or no circadian rhythm assumption can then be rejected with a PofO.OlO. Around the mesor of 1 3.44% there
is a double
change) 2.74%
(ie,
of5.65% to 8.56%.
1 108)
with
amplitude
of energy
(a measure
with a 95% confidence The acrophase is at a 95%
to - 193#{176} from midnight. cannot be demonstrated
confidence
content
ofthe
extent
interval -
interval
For metabolic (P for rhythm
167#{176}from
extending
of the
meal,
of predictable extending local
from midnight
from
-
133
rate as such, a rhythm rejection = 0.633).
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ET