Buscar

Artigo 8 revisão tcc

Faça como milhares de estudantes: teste grátis o Passei Direto

Esse e outros conteúdos desbloqueados

16 milhões de materiais de várias disciplinas

Impressão de materiais

Agora você pode testar o

Passei Direto grátis

Você também pode ser Premium ajudando estudantes

Faça como milhares de estudantes: teste grátis o Passei Direto

Esse e outros conteúdos desbloqueados

16 milhões de materiais de várias disciplinas

Impressão de materiais

Agora você pode testar o

Passei Direto grátis

Você também pode ser Premium ajudando estudantes

Faça como milhares de estudantes: teste grátis o Passei Direto

Esse e outros conteúdos desbloqueados

16 milhões de materiais de várias disciplinas

Impressão de materiais

Agora você pode testar o

Passei Direto grátis

Você também pode ser Premium ajudando estudantes
Você viu 3, do total de 6 páginas

Faça como milhares de estudantes: teste grátis o Passei Direto

Esse e outros conteúdos desbloqueados

16 milhões de materiais de várias disciplinas

Impressão de materiais

Agora você pode testar o

Passei Direto grátis

Você também pode ser Premium ajudando estudantes

Faça como milhares de estudantes: teste grátis o Passei Direto

Esse e outros conteúdos desbloqueados

16 milhões de materiais de várias disciplinas

Impressão de materiais

Agora você pode testar o

Passei Direto grátis

Você também pode ser Premium ajudando estudantes

Faça como milhares de estudantes: teste grátis o Passei Direto

Esse e outros conteúdos desbloqueados

16 milhões de materiais de várias disciplinas

Impressão de materiais

Agora você pode testar o

Passei Direto grátis

Você também pode ser Premium ajudando estudantes
Você viu 6, do total de 6 páginas

Prévia do material em texto

Circadian rhythms and meal timing: impact on energy
balance and body weight
Hedda L Boege1, Mehreen Z Bhatti1 and Marie-Pierre St-Onge1,2
Available online at www.sciencedirect.com
ScienceDirect
Energy metabolism and appetite regulating hormones follow
circadian rhythms which, when disrupted, could lead to
adverse metabolic consequences. Such circadian
misalignment, a mismatch between endogenous circadian
rhythms and behavior, is most severely experienced by shift
workers, due to nighttime wake, daytime sleep, and eating at
night. However, circadian misalignment is not restricted to shift
workers; milder shifts in sleep and mealtimes, termed social
and eating jetlag, are highly prevalent in the general population.
Social and eating jetlag result in later mealtimes, which may
promote positive energy balance and weight gain. Earlier meal
timing, specific to individual endogenous circadian patterns,
could serve to reduce cardiometabolic disease burden and aid
in weight loss and interventions should be done to test this.
Addresses
1 Sleep Center of Excellence and Division of General Medicine, Depart-
ment of Medicine, Columbia University Irving Medical Center, New York,
NY, USA
2 Institute of Human Nutrition, Columbia University Irving Medical Center,
New York, NY, USA
Corresponding author:
St-Onge, Marie-Pierre (ms2554@cumc.columbia.edu)
Current Opinion in Biotechnology 2021, 70:xx–yy
This review comes from a themed issue on Food biotechnology
Edited by Anna E Thalacker-Mercer and Martha Field
https://doi.org/10.1016/j.copbio.2020.08.009
0958-1669/ã 2020 Elsevier Ltd. All rights reserved.
Introduction
Circadian rhythms are cyclic endogenous biological pat-
terns following an �24-hour cycle that regulate the timing
of physiology, metabolism, and behavior. They initiate
wake and sleep episodes at the appropriate biological
time as well as signal feeding and fasting. When behaviors
such as eating and sleeping fail to align with circadian
cues, misalignment can occur, compromising the integrity
of robust endogenous circadian rhythms [1]. Repeated
disruption through mismatched timing of eating and
sleeping has been shown to increase the risk of obesity,
type 2 diabetes and cardiovascular disease [1,2�]. Corre-
spondingly, shift workers, who experience chronic
www.sciencedirect.com 
circadian misalignment due to complete reversal of feed-
ing-fasting and wake-sleep behavioral cycles, provide the
strongest evidence for these effects [3]. Milder desyn-
chronizing behavioral patterns, such as variability in sleep
and meal times throughout the week, are highly prevalent
in modern society and have been coined social [4] and
eating [5��] jetlag (differences in the midpoint of the
sleep or feeding episode on free days versus work days)
(Figure 1). The timing of food intake, particularly, has
come to the forefront of research efforts with studies
showing that consumption of food later in the day and
closer to bedtime is associated with higher weight status
[6,7].
While still in early stages, findings from this field of study
have broad applicability. The demands of modern life
result in many non-shift workers delaying morning meals,
adopting irregular eating patterns and extending eating
into the night [8–10]. Adjustment of meal timing in
accordance with individual endogenous circadian
rhythms could serve to reduce cardiometabolic disease
burden. Here we present evidence on the effect of meal
timing, as a disruptor of circadian rhythms, on energy
balance (energy intake and energy expenditure) and body
weight. Research to date has focused on leptin and
ghrelin as regulators of food intake, and resting energy
expenditure, all of which are known to exhibit circadian
rhythmicity [11–13].
Entrainment of circadian clocks and circadian
alignment
The endogenous circadian system is primarily controlled
by an autonomous master clock in the suprachiasmatic
nucleus (SCN) of the hypothalamus, which is synchro-
nized by ambient light and entrains secondary clocks in
the brain and most peripheral tissues of the body [2�].
Importantly, secondary clocks are also entrained by envi-
ronmental cues and behaviors, termed ‘zeitgebers,’ such
as eating and sleeping [1,2�]. When environmental and
behavioral factors are repeatedly misaligned from the
SCN-driven endogenous circadian cycle, such as when
food intake occurs during the night, integration of mis-
timed signals can disrupt the tightly controlled peripheral
system, resulting in a loss of homeostasis (circadian mis-
alignment) [2�]. Meanwhile, in conditions of circadian
alignment, behavioral cues feed into peripheral circadian
systems at the appropriate phase, facilitating the smooth
cycling of physiological processes (Figure 1). The circa-
dian rhythms of appetite regulating hormones, energy
expenditure and substrate utilization prepare the body for
Current Opinion in Biotechnology 2021, 70:1–6
mailto:ms2554@cumc.columbia.edu
https://doi.org/10.1016/j.copbio.2020.08.009
http://crossmark.crossref.org/dialog/?doi=10.1016/j.copbio.2020.08.009&domain=pdf
http://www.sciencedirect.com/science/journal/09581669
2 Food biotechnology
Figure 1
Current Opinion in Biotechnology
(a) (b)
An overview of how mistimed sleeping and eating result in circadian misalignment and the metabolic consequences.
(a) The circadian system promotes wakefulness/feeding during the biological day and sleep/fasting during the biological night.
(b) Several behavioral patterns do not fit these endogenous preferences. Shift work: Awake/feeding at night and sleeping/fasting during the day,
causing severe circadian misalignment. Social Jetlag: A shift in the midpoint of sleep on workdays versus free days, causing mild circadian
misalignment. Eating jetlag: A shift in the midpoint of the feeding episode on workdays versus free days, causing mild circadian misalignment.
These behavioral patterns result in a mismatch between the timing of eating/sleeping and the endogenous circadian system (indicated in
magenta). Circadian misalignment is thought to disrupt energy balance, resulting in increased body weight and cardiometabolic risk.
specific biological responses at different times of day to
maintain energy balance. For example, ghrelin levels are
higher in the biological evening than the morning [12],
promoting greater evening hunger. In contrast, diet
induced thermogenesis (DIT), the rise in energy expen-
diture after a meal, is higher after a morning meal than
after an isocaloric evening meal [14,15], indicating more
calories burned after a morning meal. Respiratory quo-
tient (RQ), an index of macronutrient utilization, is high-
est in the biological morning, indicative of greater carbo-
hydrate oxidation, and lowest during the biological
evening, indicating greater lipid oxidation [11,16]. These
rhythms have implications for health and mismatched
behaviors in relation to these endogenous processes can
result in adverse health effects.
Severe circadian desynchronization
Studies in mice have shown that food intake during the
biological night, akin to night shift work in humans,
causes a 12-hour shift in peripheral clock, but not central
clock, activity [17]. Such mistimed feeding results in
higher body weight [18] and increased risk of metabolic
Current Opinion in Biotechnology 2021, 70:1–6 
syndrome and diabetes [17] relative to control mice fed
during the biological day.
Studies in humans have similarly shown phase shifts in
peripheral clock activity in response to inappropriate
timing of sleep and food intake, while the phase of the
SCN master clock remains unaffected [3,19]. Chronic
shift work has been associated with metabolic disruption
and positive energy balance, resulting in increased risk of
obesity, type 2 diabetes, heart disease and metabolic
syndrome [20]. The largest body of evidence for the
impact of circadian misalignment on human health stems
from clinical interventions approximating theconditions
of shift work in healthy, non-shift working volunteers.
Acute circadian misalignment is induced via simulated
night shift or forced desynchrony protocols, in which
either active and rest phases are reversed, or the day is
artificially shortened/extended. This effectively shifts the
behavioral patterns of sleep and eating out of phase with
the endogenous rhythm of the SCN master clock, sub-
stantially altering the input received by peripheral clocks
that regulate metabolism [3].
www.sciencedirect.com
Circadian rhythms, meal timing, and body weight 3
One proposed contributor to the increased risk of obesity
observed in shift workers is higher energy intake due to
altered levels of hunger and satiety hormones ghrelin and
leptin in response to circadian misalignment. Multiple
simulated shiftwork studies observed decreased leptin
levels [21–24,25��] and increased ghrelin levels
[12,21,25��,26] in circadian misalignment relative to cir-
cadian alignment conditions. According to a recent study
[25��], these effects may be sex-dependent. Indeed, night
shift work (circadian misalignment) induced a 7%
decrease in 24-hour leptin levels and an 8% increase in
wake period ghrelin levels in females whereas in males,
leptin levels were increased by 11% and ghrelin levels
were unchanged compared to the daytime work (circadian
aligned) condition [25��]. Increased hunger and decreased
satiety in response to circadian misalignment and
depending on time of eating could contribute to weight
gain in shift workers [20] and late eaters [27]. Meanwhile,
despite higher risk of obesity and chronic disorders,
studies have not reported significant differences in energy
intake between shift and non-shift workers by objective
measure [28] or self-report [29,30,31]. However, this
could reflect inherent biases in food intake measures [32].
Whereas the influence of circadian misalignment on food
intake regulation is more conclusive, evidence related to
energy expenditure is more equivocal. A simulated night
shift intervention showed a small but significant reduc-
tion in 24-hour resting energy expenditure (REE) after
circadian misalignment compared to alignment [24],
while similar protocols produced an increase [25��] or
no effect [11,23]. The discordance in results could be
explained by the finding that REE differs greatly
between individuals but is very stable within a person
[33]. These inter-individual differences may be in part
driven by sex: Qian et al. [25��] observed distinct sex-
specific differences, with REE increasing by 4.5% in
females after circadian misalignment, while there was
no change in males.
Circadian misalignment may also affect substrate utiliza-
tion. Compared to circadian alignment, misalignment
results in reduced RQ [11,16,25��], with concomitant
lower carbohydrate oxidation [16,24] and higher lipid
oxidation [16,24]. There is some evidence that this effect
may also be sex-specific, with reduced RQ being
observed in females but not in males [25��]. In general,
the circadian system favors carbohydrate utilization in the
biological morning and lipid utilization in the biological
evening [11,16]. Circadian misalignment may cause a
potentially unfavorable shift in these patterns when con-
sidered in conjunction with other circadian-controlled
metabolic processes, such as glucose regulation. Indeed,
multiple clinical interventions have demonstrated dis-
rupted glucose-insulin metabolism in response to acute
circadian misalignment. Postprandial glucose levels are
raised in response to misaligned mealtimes and insulin
www.sciencedirect.com 
sensitivity is reduced [16,22,23], which may increase risk
of type 2 diabetes.
Milder circadian desynchronization
Epidemiological studies show that individuals with
greater social jetlag (difference in midpoint of the sleep
period between work and free days) have higher BMI,
adiposity and odds of obesity, metabolic syndrome and
type 2 diabetes [34,35]. In a study population with obe-
sity-related chronic diseases, greater social jetlag was
associated with consumption of more calories, saturated
fat and cholesterol at dinner, of more protein, total fat,
saturated fat and cholesterol at lunch, as well as more total
fat and saturated fat consumed at morning snack [36�].
Because of later waking times, social jetlag was also
associated with later mealtimes for breakfast, early after-
noon snack and dinner [36�]. These later consumption
patterns, at odds with endogenous preference, could
contribute to the observed risk of obesity in those with
greater social jetlag.
Few clinical intervention studies have explored the met-
abolic effects of mild circadian misalignment. One obser-
vational study showed that those with later midpoint of
sleep, but not necessarily social jetlag, had higher energy
intakes at dinner and after 8 PM, behaviors that were
associated with higher BMI, as well as higher intakes of
fast food, sugar-sweetened beverages, and lower fruits
and vegetables [6]. However, this study was confounded
by differences in sleep duration, whereby those with later
sleep times also had shorter sleep duration than those
with earlier sleep times. We and others have shown that
short sleep duration increases food intake [37,38].
Another study showed that sleep restriction for two nights
followed by two nights of sleep recovery and another two
nights of sleep restriction, effectively shifting midpoint of
sleep by 2.5 hours between sleep restriction and sleep
recovery, increases food intake relative to baseline, pre-
study sleep [39]. Both periods of sleep restriction
increased energy intakes by �1000 kcal whereas recovery
sleep increased intakes by �500 kcal relative to baseline.
Sex differences were observed whereby intakes were
increased similarly in the two sleep restriction periods
in both men and women, but intakes during recovery
sleep returned to baseline levels in women only. How-
ever, this study too, was confounded by differences in
sleep duration throughout the sleep conditions [39].
Our lab attempted to address this research gap via a 4-
phase randomized crossover pilot study with constant
sleep duration [40]. Six men and women underwent four
inpatient phases in which the timing, but not duration, of
sleep and meals was manipulated: Normal sleep/normal
meals, normal sleep/late meals, late sleep/normal meals
and late sleep/late meals. Sleep and mealtimes were
delayed by 3.5 hours in the late conditions relative to
those with normal times. Glucagon-like peptide
Current Opinion in Biotechnology 2021, 70:1–6
4 Food biotechnology
1 concentrations in response to a meal were higher with
early sleep and mealtimes, suggesting improved satiety
compared with the late meal condition [40]. In contrast,
earlier sleep and mealtimes were associated with higher
ghrelin concentrations and did not influence leptin con-
centrations. The combination of normal sleep and meal-
times had a reducing effect on food intakes [40]. Although
limited, these studies suggest a potential influence of
small shifts in sleep and meal timing on regulation of
energy balance. We are not aware of any study that has
assessed the influence of social jetlag on REE.
Meal timing and weight status
Outside of the laboratory, several recent epidemiological
studies have examined the association between timing of
eating and obesity risk. Eating jetlag, the difference in
midpoint of the eating period between work and free
days, has been associated with higher BMI [5��]. In this
epidemiological sample, eating jetlag was driven primar-
ily by a delay in breakfast time on weekends relative to
weekdays. Later meal timing in general has been associ-
ated with higher daily caloric intakes [27] and higher
BMI, independent of sleep timing and duration [6]. Xiao
et al. [7] associated a higher percentage of dietary intake in
the morning with 50% lower odds of overweight or
obesity, while a higherpercentage of dietary intake in
the evening was associated with 80% higher odds of
overweight or obesity.
A study by Bandı́n et al. [41] in which mealtimes were
delayed by 3.5 hours while sleep was kept constant,
showed decreased pre-meal REE, decreased fasting
RQ and decreased carbohydrate oxidation compared to
the control condition. Other studies have shown that diet-
induced thermogenesis (DIT), the rise in energy expen-
diture in response to food intake, is consistently lower in
response to an evening meal compared with a morning
meal [14,15,24]. In fact, one study reported 44% lower
DIT following an evening meal compared to a morning
meal [15]. These findings suggest that energy homeosta-
sis is favored when greater caloric intakes occur in the
morning/early afternoon versus the evening/night due to
higher energy costs of processing foods consumed at an
earlier time.
Importantly, meal timing patterns may not follow a ‘one-
size-fits-all’ approach. Recent findings suggest that timing
of meals relative to individual circadian clock timing,
marked by evening melatonin onset, is a better predictor
of body composition and weight status than clock time
[42,43��]. Indeed, individuals consuming a greater pro-
portion of their daily energy intakes closer to melatonin
onset (circadian clock) had higher BMI and percentage
body fat than those who consumed food earlier in their
biological day [42]. The same study showed that individ-
uals with higher percentage body fat ate 8% more of their
total daily calories in the biological evening, and 13%
Current Opinion in Biotechnology 2021, 70:1–6 
more carbohydrates in the biological afternoon, irrespec-
tive of clock hour, than individuals with lower percentage
body fat [43��]. Given the circadian rhythmicity of DIT
and substrate oxidation highlighted above, food con-
sumption later in the day could result in fewer calories
burned and greater carbohydrates remaining in circula-
tion, increasing the risk of weight gain and type 2 diabetes
in susceptible individuals.
Meal timing and weight loss
Given the associations between timing of food intake and
circadian alignment, it is plausible that shifting mealtimes
could influence weight management. Indeed, behavioral
weight loss programs have shown that greater weight loss
occurs in those who consume their main daily meal earlier
in the day compared to those who consume that meal later
in the day [44] and in those who consume the greatest
percentage of daily calories during a morning meal [45–
48]. A six-year follow-up study of bariatric surgery simi-
larly associated earlier consumption of the main meal with
greater weight loss success compared to a later main meal,
an observation that could not be explained by differences
in energy intake, diet composition or sleep duration [49].
These results indicate that the timing of meals and
distribution of caloric intake throughout the day may
be important considerations for weight management,
along with traditional dietary characteristics such as
energy intake and diet composition.
Conclusion
Circadian misalignment is increasingly recognized as a
risk factor for obesity and cardiometabolic disease. While
shift workers are most affected, there is a growing under-
standing that milder shifts in eating and sleeping patterns,
such as social jetlag and eating jetlag, can also have
adverse health consequences. Both social and eating jet-
lags result in later meal consumption patterns, which may
result in eating at biologically unfavorable times for
energy and macronutrient metabolism. Clinical interven-
tion studies assessing the effects of these subtle shifts in
sleep and meal timing are needed to uncover the mecha-
nism by which mild forms of circadian misalignment lead
to higher body weight and cardiometabolic risk. Finally,
due to inter-individual differences in circadian timing, it
may be important to personalize meal timing recommen-
dations. Meal timing in relation to chronotype, a measure
of innate individual preference for morning or evening
shown to modulate the risk associated with late eating
[50], could be considered to alleviate burden in those at
high risk. An understanding of circadian rhythms and
differential metabolic responses to food intake at differ-
ent circadian phases can inform recommendations for
temporally healthier eating patterns and should be the
subject of clinical investigations.
Conflict of interest statement
Nothing declared.
www.sciencedirect.com
Circadian rhythms, meal timing, and body weight 5
Acknowledgements
This was funded in part by the National Institutes of Health [grant numbers
R01 HL142648, R01 HL128226] and the American Heart Association [grant
number 16SFRN27950012] (St-Onge).
References and recommended reading
Papers of particular interest, published within the period of review,
have been highlighted as:
� of special interest
�� of outstanding interest
1. Buijs FN, León-Mercado L, Guzmán-Ruiz M, Guerrero-Vargas NN,
Romo-Nava F, Buijs RM: The circadian system: a regulatory
feedback network of periphery and brain. Physiology 2016,
31:170-181.
2.
�
Challet E: The circadian regulation of food intake. Nat Rev
Endocrinol 2019, 15:393-405
A comprehensive review detailing the entrainment of circadian rhythms,
circadian control of food intake and circadian desynchrozing factors.
3. Pickel L, Sung H-K: Feeding rhythms and the circadian
regulation of metabolism. Front Nutr 2020, 7.
4. Wittmann M, Dinich J, Merrow M, Roenneberg T: Social jetlag:
misalignment of biological and social time. Chronobiol Int 2006,
23:497-509.
5.
��
Zerón-Rugerio M, Hernáez Á, Porras-Loaiza A, Cambras T,
Izquierdo-Pulido M: Eating jet lag: a marker of the variability in
meal timing and its association with body mass index.
Nutrients 2019, 11:2980
Coined the term ‘eating jetlag’ to describe the difference in the midpoint of
the eating period between work and free days, a mild form of circadian
misalignment.
6. Baron KG, Reid KJ, Kern AS, Zee PC: Role of sleep timing in
caloric intake and BMI. Obesity 2011, 19:1374-1381.
7. Xiao Q, Garaulet M, Scheer FAJL: Meal timing and obesity:
interactions with macronutrient intake and chronotype. Int J
Obes 2019, 43:1701-1711.
8. Gill S, Panda S: A smartphone app reveals erratic diurnal eating
patterns in humans that can be modulated for health benefits.
Cell Metab 2015, 22:789-798.
9. St-Onge M-P, Ard J, Baskin ML, Chiuve SE, Johnson HM, Kris-
Etherton P, Varady K: Meal timing and frequency: implications
for cardiovascular disease prevention: a scientific statement
from the american heart association. Circulation 2017, 135:e96-
e121.
10. Eicher-Miller HA, Khanna N, Boushey CJ, Gelfand SB, Delp EJ:
Temporal dietary patterns derived among the adult
participants of the national health and nutrition examination
survey 1999-2004 are associated with diet quality. J Acad Nutr
Diet 2016, 116:283-291.
11. Zitting K-M, Vujovic N, Yuan RK, Isherwood CM, Medina JE,
Wang W, Buxton OM, Williams JS, Czeisler CA, Duffy JF: Human
resting energy expenditure varies with circadian phase. Curr
Biol 2018, 28:3685-3690.e3683.
12. Qian J, Morris CJ, Caputo R, Garaulet M, Scheer FAJL: Ghrelin is
impacted by the endogenous circadian system and by
circadian misalignment in humans. Int J Obes 2019, 43:1644-
1649.
13. Shea SA, Hilton MF, Orlova C, Ayers RT, Mantzoros CS:
Independent circadian and sleep/wake regulation of
adipokines and glucose in humans. J Clin Endocrinol Metab
2005, 90:2537-2544.
14. Bo S, Fadda M, Castiglione A, Ciccone G, De Francesco A,
Fedele D, Guggino A, Parasiliti Caprino M, Ferrara S, Vezio
Boggio M et al.: Is the timing of caloric intake associated with
variation in diet-induced thermogenesis and in the metabolic
pattern? A randomized cross-over study. Int J Obes 2015,
39:1689-1695.
www.sciencedirect.com 
15. Morris CJ, Garcia JI, Myers S, Yang JN, Trienekens N,
Scheer FAJL: The human circadian system has a dominating
role incausing the morning/evening difference in diet-induced
thermogenesis. Obesity 2015, 23:2053-2058.
16. Morris CJ, Yang JN, Garcia JI, Myers S, Bozzi I, Wang W,
Buxton OM, Shea SA, Scheer FAJL: Endogenous circadian
system and circadian misalignment impact glucose tolerance
via separate mechanisms in humans. Proc Natl Acad Sci U S A
2015, 112:E2225-E2234.
17. Mukherji A, Kobiita A, Damara M, Misra N, Meziane H, Champy M-
F, Chambon P: Shifting eating to the circadian rest phase
misaligns the peripheral clocks with the master SCN clock and
leads to a metabolic syndrome. Proc Natl Acad Sci U S A 2015,
112:E6691-E6698.
18. Arble DM, Bass J, Laposky AD, Vitaterna MH, Turek FW:
Circadian timing of food intake contributes to weight gain.
Obesity 2009, 17:2100-2102.
19. Wehrens SMT, Christou S, Isherwood C, Middleton B, Gibbs MA,
Archer SN, Skene DJ, Johnston JD: Meal timing regulates the
human circadian system. Curr Biol 2017, 27:1768-1775.e1763.
20. Kervezee L, Kosmadopoulos A, Boivin DB: Metabolic and
cardiovascular consequences of shift work: the role of
circadian disruption and sleep disturbances. Eur J Neurosci
2020, 51:396-412.
21. Buxton OM, Cain SW, O’Connor SP, Porter JH, Duffy JF, Wang W,
Czeisler CA, Shea SA: Adverse metabolic consequences in
humans of prolonged sleep restriction combined with
circadian disruption. Sci Transl Med 2012, 4:129ra.
22. Scheer FAJL, Hilton MF, Mantzoros CS, Shea SA: Adverse
metabolic and cardiovascular consequences of circadian
misalignment. Proc Natl Acad Sci U S A 2009, 106:4453-4458.
23. Gonnissen HK, Rutters F, Mazuy C, Martens EA, Adam TC,
Westerterp-Plantenga MS: Effect of a phase advance and phase
delay of the 24-h cycle on energy metabolism, appetite, and
related hormones. Am J Clin Nutr 2012, 96:689-697.
24. McHill AW, Melanson EL, Higgins J, Connick E, Moehlman TM,
Stothard ER, Wright KP: Impact of circadian misalignment on
energy metabolism during simulated nightshift work. Proc Natl
Acad Sci U S A 2014, 111:17302-17307.
25.
��
Qian J, Morris CJ, Caputo R, Wang W, Garaulet M, Scheer FAJL:
Sex differences in the circadian misalignment effects on
energy regulation. Proc Natl Acad Sci U S A 2019, 116:23806-
23812
The first study to identify distinct sex-specific differences in circadian
misalignment’s effects on REE, RQ and appetite regulating hormones
leptin and ghrelin. Suggests that circadian misalignment may affect
energy balance in men and women through separate mechanisms.
26. Schiavo-Cardozo D, Lima MMO, Pareja JC, Geloneze B:
Appetite-regulating hormones from the upper gut: disrupted
control of xenin and ghrelin in night workers. Clin Endocrinol
2013, 79:807-811.
27. Reid KJ, Baron KG, Zee PC: Meal timing influences daily caloric
intake in healthy adults. Nutr Res 2014, 34:930-935.
28. Chen Y, Lauren S, Chang BP, Shechter A: Objective food intake
in night and day shift workers: a laboratory study. Clocks Sleep
2018, 1:42-49.
29. Cayanan EA, Eyre NAB, Lao V, Comas M, Hoyos CM, Marshall NS,
Phillips CL, Shiao JSC, Guo Y-LL, Gordon CJ: Is 24-hour energy
intake greater during night shift compared to non-night shift
patterns? A systematic review. Chronobiol Int 2019, 36:1599-
1612.
30. Shaw E, Dorrian J, Coates AM, Leung GKW, Davis R,
Rosbotham E, Warnock R, Huggins CE, Bonham MP: Temporal
pattern of eating in night shift workers. Chronobiol Int 2019,
36:1613-1625.
31. Lauren S, Chen Y, Friel C, Chang B, Shechter A: Free-living sleep,
food intake, and physical activity in night and morning shift
workers. J Am College Nutr 2020, 39:450-456.
Current Opinion in Biotechnology 2021, 70:1–6
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0005
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0005
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0005
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0005
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0010
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0010
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0015
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0015
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0020
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0020
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0020
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0025
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0025
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0025
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0025
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0030
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0030
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0035
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0035
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0035
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0040
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0040
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0040
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0045
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0045
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0045
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0045
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0045
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0050
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0050
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0050
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0050
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0050
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0055
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0055
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0055
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0055
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0060
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0060
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0060
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0060
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0065
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0065
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0065
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0065
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0070
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0070
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0070
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0070
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0070
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0070
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0075
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0075
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0075
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0075
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0080
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0080
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0080
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0080
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0080
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0085
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0085
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0085
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0085
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0085
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0090
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0090
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0090
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0095
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0095
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0095
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0100
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0100
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0100
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0100
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0105http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0105
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0105
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0105
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0110
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0110
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0110
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0115
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0115
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0115
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0115
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0120
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0120
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0120
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0120
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0125
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0125
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0125
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0125
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0130
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0130
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0130
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0130
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0135
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0135
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0140
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0140
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0140
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0145
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0145
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0145
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0145
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0145
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0150
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0150
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0150
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0150
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0155
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0155
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0155
6 Food biotechnology
32. Subar AF, Freedman LS, Tooze JA, Kirkpatrick SI, Boushey C,
Neuhouser ML, Thompson FE, Potischman N, Guenther PM,
Tarasuk V et al.: Addressing current criticism regarding the
value of self-report dietary data. J Nutr 2015, 145:2639-2645.
33. Melanson EL, Ritchie HK, Dear TB, Catenacci V, Shea K,
Connick E, Moehlman TM, Stothard ER, Higgins J, McHill AW
et al.: Daytime bright light exposure, metabolism, and
individual differences in wake and sleep energy expenditure
during circadian entrainment and misalignment. Neurobiol
Sleep Circadian Rhythms 2018, 4:49-56.
34. Parsons MJ, Moffitt TE, Gregory AM, Goldman-Mellor S,
Nolan PM, Poulton R, Caspi A: Social jetlag, obesity and
metabolic disorder: investigation in a cohort study. Int J Obes
2015, 39:842-848.
35. Koopman ADM, Rauh SP, Van ‘T Riet E, Groeneveld L, Van Der
Heijden AA, Elders PJ, Dekker JM, Nijpels G, Beulens JW,
Rutters F: The association between social jetlag, the metabolic
syndrome, and Type 2 diabetes mellitus in the general
population: the new hoorn study. J Biol Rhythms 2017, 32:359-
368.
36.
�
Mota MC, Silva CM, Balieiro LCT, Gonç alves BF, Fahmy WM,
Crispim CA: Association between social jetlag food
consumption and meal times in patients with obesity-related
chronic diseases. PLoS One 2019, 14 e0212126
An epidemiological study associating social jetlag with later meal timing
throughout the day, higher caloric intakes, and a poorer diet (higher total
fat, saturated fat and cholesterol intakes) compared to individuals with no
social jetlag.
37. St-Onge M-P, Roberts AL, Chen J, Kelleman M, O’Keeffe M,
Roychoudhury A, Jones PJ: Short sleep duration increases
energy intakes but does not change energy expenditure in
normal-weight individuals. Am J Clin Nutr 2011, 94:410-416.
38. Al Khatib HK, Harding SV, Darzi J, Pot GK: The effects of partial
sleep deprivation on energy balance: a systematic review and
meta-analysis. Eur J Clin Nutr 2017, 71:614-624.
39. Depner CM, Melanson EL, Eckel RH, Snell-Bergeon JK,
Perreault L, Bergman BC, Higgins JA, Guerin MK, Stothard ER,
Morton SJ et al.: Ad libitum weekend recovery sleep fails to
prevent metabolic dysregulation during a repeating pattern of
insufficient sleep and weekend recovery sleep. Curr Biol 2019,
29:957-967.e954.
40. St-Onge MP, Pizinger T, Kovtun K, RoyChoudhury A: Sleep and
meal timing influence food intake and its hormonal regulation
in healthy adults with overweight/obesity. Eur J Clin Nutr 2019,
72:76-82.
Current Opinion in Biotechnology 2021, 70:1–6 
41. Bandı́n C, Scheer FAJL, Luque AJ, Ávila-Gandı́a V, Zamora S,
Madrid JA, Gómez-Abellán P, Garaulet M: Meal timing affects
glucose tolerance, substrate oxidation and circadian-related
variables: a randomized, crossover trial. Int J Obes 2015,
39:828-833.
42. McHill AW, Phillips AJ, Czeisler CA, Keating L, Yee K, Barger LK,
Garaulet M, Scheer FA, Klerman EB: Later circadian timing of
food intake is associated with increased body fat. Am J Clin
Nutr 2017, 106:1213-1219.
43.
��
McHill A, Czeisler C, Phillips A, Keating L, Barger L, Garaulet M,
Scheer F, Klerman E: Caloric and macronutrient intake differ
with circadian phase and between lean and overweight young
adults. Nutrients 2019, 11:587
This study found that individual circadian phase better predicted the
metabolic effects of meal timing than clock time, due to differences in
timing of circadian rhythms between individuals. This suggests that
recommendations for dietary patterns might be most effective if perso-
nalized to an individual’s endogenous circadian cycle.
44. Garaulet M, Gómez-Abellán P, Alburquerque-Béjar JJ, Lee YC,
Ordovás JM, Scheer FAJL: Timing of food intake predicts
weight loss effectiveness. Int J Obes 2013, 37:604-611.
45. Jakubowicz D, Barnea M, Wainstein J, Froy O: High caloric intake
at breakfast vs. dinner differentially influences weight loss of
overweight and obese women. Obesity 2013, 21:2504-2512.
46. Raynor HA, Li F, Cardoso C: Daily pattern of energy distribution
and weight loss. Physiol Behav 2018, 192:167-172.
47. Kahleova H, Lloren JI, Mashchak A, Hill M, Fraser GE: Meal
frequency and timing are associated with changes in body
mass index in adventist health study 2. J Nutr 2017, 147:1722-
1728.
48. Lombardo M, Bellia A, Padua E, Annino G, Guglielmi V,
D’Adamo M, Iellamo F, Sbraccia P: Morning meal more efficient
for fat loss in a 3-month lifestyle intervention. J Am College Nutr
2014, 33:198-205.
49. Ruiz-Lozano T, Vidal J, De Hollanda A, Scheer FAJL, Garaulet M,
Izquierdo-Pulido M: Timing of food intake is associated with
weight loss evolution in severe obese patients after bariatric
surgery. Clin Nutr 2016, 35:1308-1314.
50. Muñoz JSG, Cañavate R, Hernández CM, Cara-Salmerón V,
Morante JJH: The association among chronotype, timing of
food intake and food preferences depends on body mass
status. Eur J Clin Nutr 2017, 71:736-742.
www.sciencedirect.com
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0160
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0160
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0160
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0160
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0165
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0165
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0165
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0165
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0165
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0165
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0170
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0170
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0170
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0170http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0175
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0175
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0175
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0175
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0175
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0175
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0180
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0180
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0180
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0180
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0185
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0185
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0185
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0185
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0190
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0190
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0190
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0195
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0195
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0195
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0195
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0195
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0195
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0200
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0200
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0200
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0200
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0205
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0205
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0205
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0205
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0205
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0210
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0210
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0210
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0210
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0215
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0215
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0215
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0215
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0220
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0220
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0220
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0225
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0225
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0225
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0230
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0230
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0235
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0235
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0235
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0235
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0240
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0240
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0240
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0240
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0245
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0245
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0245
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0245
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0250
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0250
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0250
http://refhub.elsevier.com/S0958-1669(20)30116-6/sbref0250
	Circadian rhythms and meal timing: impact on energy balance and body weight
	Introduction
	Entrainment of circadian clocks and circadian alignment
	Severe circadian desynchronization
	Milder circadian desynchronization
	Meal timing and weight status
	Meal timing and weight loss
	Conclusion
	Conflict of interest statement
	References and recommended reading
	Acknowledgements

Continue navegando