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Proceedings of the Nutrition Society (2016), 75, 464474 doi:10.

1017/S0029665116000318
The Authors 2016 First published online 13 June 2016. This is an Open Access article,
distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.
org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any
medium, provided the original work is properly cited.

The Joint Winter Meeting between the Nutrition Society and the Royal Society of Medicine held at The Royal Society of Medicine,
London on 89 December 2015

Conference on Roles of sleep and circadian rhythms in the origin and nutritional
management of obesity and metabolic disease
Cuthbertson Medal Lecture

Is breakfast the most important meal of the day?


Proceedings of the Nutrition Society

James A. Betts1*{, Enhad A. Chowdhury1{, Javier T. Gonzalez1, Judith D. Richardson1,


Kostas Tsintzas2 and Dylan Thompson1
1
Department for Health, University of Bath, Bath BA2 7AY, UK
2
School of Life Sciences, Queens Medical Centre, University of Nottingham, Nottingham NG7 2UH, UK

The Bath Breakfast Project is a series of randomised controlled trials exploring the effects of
extended morning fasting on energy balance and health. These trials were categorically not
designed to answer whether or not breakfast is the most important meal of the day.
However, this review will philosophise about the meaning of that question and about
what questions we should be asking to better understand the effects of breakfast, before sum-
marising how individual components of energy balance and health respond to breakfast v.
fasting in lean and obese adults. Current evidence does not support a clear effect of regularly
consuming or skipping breakfast on body mass/composition, metabolic rate or diet-induced
thermogenesis. Findings regarding energy intake are variable, although the balance of evi-
dence indicates some degree of compensatory feeding later in the day such that overall en-
ergy intake is either unaffected or slightly lower when breakfast is omitted from the diet.
However, even if net energy intake is reduced, extended morning fasting may not result in
expected weight loss due to compensatory adjustments in physical activity thermogenesis.
Specically, we report that both lean and obese adults expended less energy during the
morning when remaining in the fasted state than when consuming a prescribed breakfast.
Further research is required to examine whether particular health markers may be respon-
sive to breakfast-induced responses of individual components of energy balance irrespective
of their net effect on energy balance and therefore body mass.

Fasting: Energy balance: Health: Thermogenesis

The broad eld of nutrition and health is rife with myths, considered in the present review and both absolutely
misconceptions and frequently posed yet seemingly fun- yes (just as a second is a second, one thermochemical
damental questions that we intuitively feel should have calorie is simply a unit of measurement equivalent to
simple answers. Is a calorie a calorie? Is obesity due to 418 J). The third is not so easily answered and there
eating too much or doing too little? Is breakfast the can be no correct response until we rene that question;
most important meal of the day? Often there are simple If you wish to converse with me said Voltaire dene
answers, the rst two being central to the themes your terms. In this case, we must dene both what is

Abbreviations: DIT, diet-induced thermogenesis.


*Corresponding author: Dr J. Betts, email j.betts@bath.ac.uk
{Joint rst authors.

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http://dx.doi.org/10.1017/S0029665116000318
Extended morning fasting, energy balance and health 465

meant by breakfast and what is meant by important (i.e. of the many highly caloric beverages available, yet (not-
important for what?). withstanding differences in gastric emptying rate and
Framing our question in terms of whether breakfast is metabolic response to different nutrients in solid v. liquid
the most important meal of the day also implies some in- form(6)), our net energy balance does not discriminate be-
herent value in comparing breakfast with other daily eat- tween absorbed nutrients or calories depending on
ing occasions. Why should the potential benets of whether they required chewing; a calorie is a calorie.
breakfast and therefore our decision about breakfast con- While in the future it might become possible to justify
sumption depend on the relative importance of lunch or a rationale for dening meals based on a certain mixture
dinner? For example, breakfast consumption is unlikely of nutrients, a logical starting point to dene the essential
to be more important for our general health than physic- conditions of breakfast per se would be based on the
al exercise or not smoking but that does not discount that quantity and timing of energy consumed. We propose
breakfast may be sufciently important to form part of a that a quantity of 2092 kJ (50 kcal) represents an appro-
wider healthy lifestyle(14). Indeed, markers of a healthy priate arbitrary threshold to exclude common ingestive
lifestyle are associated with frequent breakfast consump- behaviours that would neither be recognised as a meal
tion, which confounds interpretation of causal links by the majority of people nor meaningfully shift our
between breakfast and good health. physiology towards the fed-state, a marker of which
The true question to be explored in the present review could be a detectable perturbation in exogenous and/or
therefore concerns our daily decision about when to endogenous substrate utilisation (thus one standard tea/
Proceedings of the Nutrition Society

interrupt an extended period of fasting (e.g. overnight). coffee would be unlikely to meet this criterion).
Whether what might then be dened as breakfast and The issue of timing is more complex and can be con-
has the potential to cause meaningful effects on various sidered relative to time of day, time of waking and/or
health markers across different populations and contexts the intervals that distinguish separate eating occasions.
can then be considered. While this approach is unlikely A universal denition of breakfast as morning feeding
to t the false dichotomy through which the media obses- based purely on lightdark cycles (i.e. clock time) independ-
sively brand any given health strategy as universally good ent of sleepwakes cycles (or vice versa) is complicated by
or bad, the truth is understandably less extreme or con- variance in these very cycles due to geographical/seasonal
sistent (i.e. breakfast is probably more or less important differences in daylight hours or cultural/vocational differ-
for some outcomes/people per day than for others). ences in sleeping patterns (e.g. night-shift workers). A nom-
inal period of 2 h after waking is also often applied to the
denition of the breakfast meal, with separate meals in
What do we mean by Breakfast? turn having been distinguished from snacks by a cut-off
quantity of approximately 10878 kJ (260 kcal) and distinct
One issue contributing to the apparently conicting eating occasions isolated on the basis of a 45 min interval(7).
ndings in this area is that there is no universally accepted On balance, it therefore seems reasonable for a working
denition of breakfast(5); and why should there be? denition of breakfast to represent the rst meal consumed
Without thinking about this too hard, it might at rst within 2 h after the longest sleep in any 24 h period, thus nor-
seem logical simply to dene breakfast as the rst meal mally also reecting the longest daily duration spent in the
of the day. This is then consistent with the etymology to fasted-state and the only time most of us are genuinely
break the fast and may work for some as a general de- post-absorptive(8).
scription of breakfast but is logically awed and not overly According to the earlier rationale, our research involved
helpful as a scientic denition. Consider an individual approximately 70 lean and obese adults, of whom none
who breaks their fast shortly after waking by ingesting en- worked night-shifts and approximately one-third habit-
ergy from carbohydrate, protein and fat in the form of cof- ually consumed <2092 kJ (50 kcal) within 2 h of waking
fee with milk and sugar, then nothing else until on most days, so might be classied as breakfast skippers.
early-afternoon when the same mixed-macronutrients These individuals kindly participated in a series of experi-
(plus alcohol) are consumed but this time in the form of ments known as the Bath Breakfast Project, in which we
spaghetti Bolognese and wine. Opinions may now be allocated the habitual breakfast consumers and skippers
divided about whether this person had breakfast at all equally into groups who for 6 weeks either: extended
and, if so, whether it was coffee and/or spaghetti and their overnight fast (0 kJ) until midday everyday; con-
wine. Can we count a cup of coffee as a meal? Was the spa- sumed 14644 kJ (350 kcal) within 2 h of waking and at
ghetti consumed in the fasted-state (i.e. post-absorptive)? least 29288 kJ (700 kcal) before 11.00 hours everyday;
What if we learn that this person woke at midday? or maintained their usual lifestyles for 6 weeks(9).
These differences of opinion become problematic when In contrast to the wealth of evidence contrasting differ-
scientic investigations have surveyed breakfast habits or ent types or amounts of breakfast foods, this is the rst ran-
recommended breakfast consumption but allowed indi- domised controlled trial to compare a treatment involving
vidual interpretation regarding what constitutes breakfast. breakfast with the complete absence of morning feeding in
This can be informative from a sociological perspective relation to all components of energy balance. Whilst the
but it is helpful when considering physiological health project therefore ostensibly concerns breakfast (indeed,
effects to employ a more precise and consistent operation- you may only be reading the present paper due to a shared
al denition. Taking the earlier example, some studies interest in that meal), our intervention from a basic science
have included only solid foods as breakfast irrespective perspective is in fact the fasting treatment, with morning

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466 J. A. Betts et al.

feeding serving as a control (Bath Extended Morning has been veried can be described as gratuitous,
Fasting Project did not seem so catchy). On that basis, conrmatory studies continue to emerge even today des-
the precise composition of breakfast prescribed was less pite the stated relationship conrmed by meta-analysis at
important at this stage than simply ensuring that whatever a condence level of P = 0001 almost 20 years ago (ris-
was ingested differed sufciently from fasting that mean- ing to P < 1042 at the most recent cut-off in 2011)(11).
ingful effects would be detectable should they exist. The There can be little doubt, therefore, that individuals
added practical benets of this initial approach are that who more frequently consume breakfast tend to be leaner
any signicant effects could be generalised more broadly and that this pattern hardly varies across a diverse range
as responses to fasting as opposed to the presence or ab- of human populations. However, no matter how strong
sence of specic foods consumed at breakfast; whereas these correlations may be, they cannot be used to draw
none could argue that these treatments fail to polarise a causal inference and so cannot inform evidence-based
the contrast and meet all but the most extreme and unusual recommendations either encouraging or discouraging
denitions of breakfast. breakfast for the purposes of weight-management.
The Bath Breakfast Project was designed primarily to
examine individual components of energy balance as
What do we mean by Important? opposed to long-term weight-change, as evident in the
fact that the intervention was applied for only 6 weeks
If you are hungry upon waking and personally prefer to with direct prescription and adherence to the treatments
Proceedings of the Nutrition Society

promptly satiate your hunger, then breakfast is undoubt- (i.e. a completers-only analysis)(9). In this sense, our
edly the most important (i.e. only) meal suited to that examination of body mass changes as an indication of
purpose. Similarly, if your morning will involve physical net energy (im)balance better reects an efcacy trial
exercise with performance on that day a priority, then and nicely complements the results of a concurrent effect-
consuming a carbohydrate-rich breakfast is the most im- iveness trial which reported no signicant difference in
portant meal to achieve your immediate goals(10). weight-loss over 16 weeks with a recommendation to
However, if we place importance on long-term health eat or skip breakfast (i.e. an intention-to-treat ana-
outcomes, these generally do not respond acutely to a lysis)(13). Our data are consistent with this conclusion in
single food or meal but instead require sustained expos- that there was no signicant difference in total body
ure to a consistent dietary pattern. In this case, we are mass change between breakfast v. fasting amongst indivi-
asking whether regular daily breakfast has a chronic ef- duals who were either lean(14) or obese(15), although it is
fect on energy balance and associated health outcomes. interesting to contrast the pattern of changes in dual-
The present review will sequentially consider the effects of energy x-ray absorptiometry-derived body composition
breakfast v. extended morning fasting on the various indi- between groups across both levels of adiposity (Fig. 1).
vidual components of energy balance and health. For each As can be seen, despite the absence of differences be-
outcome, we will rst summarise the state of evidence link- tween groups according to the breakfast intervention,
ing breakfast to energy balance prior to our recent rando- there were signicant within-group changes from base-
mised controlled trial. That is the evidence upon which the line but with the pattern reversed according to adiposity
pervasive societal beliefs about breakfast rested(11), despite and treatment group. Specically working from left to
being almost entirely cross-sectional in nature. The vast right across Fig. 1, lean individuals in the fasting group
and diverse populations surveyed are a legitimate strength did not compensate for the energy missed at breakfast,
of these epidemiological studies but are also responsible hence there is a signicant reduction in body mass (most-
for misconceptions amongst a public (and media) ly from fat loss); whereas lean individuals in the breakfast
ill-equipped to evaluate research design, measurement group certainly do not gain weight despite the relatively
error or controls, so who are inclined only to believe the large prescription of at least 29288 kJ (700 kcal) by
ndings (or headlines) from studies perceived to be large 11.00 hours daily for 6 weeks(14). In contrast, it was the
(again, dene your terms). Conversely, other studies are fasting group in the obese population who exhibited
too often discounted for being small irrespective of accuracy the greatest compensation, with avoidance of weight-loss
and precision in measurement (for a primer see How big despite consuming not a single calorie until midday every
does my sample need to be?(12)), which means we sometimes day for 6 weeks; whereas the obese individuals in the
miss the opportunity to complement epidemiology with breakfast group clearly did not compensate by expending
causal evidence from focused, tightly controlled and prop- the prescribed energy intake (or reducing subsequent en-
erly powered experiments (i.e. research where interventions ergy intake sufciently) and so increased energy storage
and controls are directly manipulated). We will therefore in the form of adipose tissue(15).
set-out here how our understanding of causality specic The net effect of the earlier pattern is that, whether fed
to each outcome has been advanced by our recent series or fasted in the mornings, lean individuals may favour a
of randomised controlled trials; the Bath Breakfast Project. more negative energy balance and obese individuals a
more positive energy balance. This could mean that an
individuals natural propensity to compensate is what
Body mass/composition determines the extent of adiposity and/or could equally
mean that the extent of adiposity determines compensa-
As recently reviewed, although the extent to which the tion. Whichever is the case, we begin to question both
mere association between breakfast omission and obesity whether breakfast recommendations should vary

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Extended morning fasting, energy balance and health 467
Proceedings of the Nutrition Society

Fig. 1. Changes in dual-energy x-ray absorptiometry-derived body composition amongst lean(14) and obese(15) adults over 6 weeks
with either ingestion of 29288 kJ (700 kcal) before 11.00 hours daily (Breakfast group), abstinence from all energy-providing nutrients
until at least 12.00 hours daily (Fasting group) or lifestyle maintenance (Control). Data are means with SE bars and * denotes a
signicant within group change from baseline (P < 005).

according to adiposity and what mechanisms are metabolic measurements, subjective responses and appetite
involved in compensation (i.e. which components of en- regulatory hormones, which can provide valuable
ergy balance are responsible)? mechanistic insight(23). The majority of appetite regulatory
hormones previously measured are related to satiety and
satiation (e.g. peptide tyrosine-tyrosine (PYY), glucagon-
like peptide-1, leptin) but ghrelin acts as an appetite
Components of energy balance stimulant(24). As would be expected, there are clear
Energy intake differences between morning fasting and breakfast
consumption during the morning, with a postprandial
Cross-sectional observations. Omission of breakfast
reduction in ghrelin and increased PYY in response to
results in an energy intake decit at the beginning of
breakfast consumption(25,26), thus reecting an
the day relative to breakfast consumption. Whether
anorexigenic response evidenced by subjective measures of
this decit is maintained will depend on the existence/
appetite, as recently reviewed in this Journal(27).
magnitude of compensatory feeding throughout the
Lunchtime feeding also elicits a PYY response that
remainder of the day. Cross-sectional evidence
persists throughout the afternoon(25,26), suggesting that
predominantly suggests lower energy intake in those
this hormone reects total cumulative intake as opposed
that skip breakfast (1619), with a recent within person
to the energy content of the most recent meal. In con-
analysis from The National Health and Nutrition
trast, both Clayton et al.(28) and our recent studies in
Examination Survey showing that energy intake is
lean(25) and obese(26) individuals suggest that, paradoxic-
10334 kJ (247 (95 % CI 121, 373) kcal) lower for
ally, acylated ghrelin remains elevated during the after-
men and 7824 kJ (187 (95 % CI 121, 253) kcal) lower
noon in those that have consumed a carbohydrate-rich
for women on days when breakfast was omitted (both
breakfast and lunch. This may be related to the reduced
P < 0001)(20). However, this observation has not been
insulinaemic response to the lunchtime meal due to the
consistent across all studies(3), with work categorising
second-meal effect(29). While these ndings for hormonal
individuals by graded breakfast frequency reporting
appetite regulatory mechanisms and results of subjective
no difference despite varying category denitions(2,4,21).
appetite assessments are informative, it is important to
Acute laboratory studies. Experimental research has acknowledge that numerous factors contribute to appe-
examined energy intake in both tightly-controlled acute tite regulation(30). We have also shown in obese indivi-
settings in the laboratory and with chronic exposure to duals that the pattern of appetite regulatory hormones
different morning feeding interventions under free-living and subjective appetite ratings does not necessarily pre-
conditions (i.e. people studied in their usual environment). dict ad libitum intake(26).
The nature of laboratory investigations allows precise Studies investigating acute appetite regulation follow-
control and measurement of actual intake, yet it is that ing breakfast omission fall into two main categories:
same tight control and elimination of external inuences those that have examined subsequent ad libitum energy
that presents a limitation when generalising to real world intake following an unbroken overnight fast; and those
behaviours(22). However, laboratory investigations allow where prior to lunch a pre-lunch snack (i.e. preload)
measurement of other relevant variables such as concurrent was provided in both breakfast consumption/omission

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468 J. A. Betts et al.

conditions such that lunch was always consumed in a fed consuming 29288 kJ (700 kcal) by 11.00 hours, with
state. In studies of lean individuals where lunch was con- at least half of this consumed within 2 h of waking(9).
sumed ad libitum, most but not all(31,32) indicate energy In lean individuals we found evidence for limited dietary
intake is increased at the lunch meal, both when compensation, with the breakfast group consuming
fasted(25,28,31) and after a morning preload(33). Of these 22551 kJ/d (539 (95 % CI 157, 920) kcal/d) more than
studies, Astbury et al. report the energy decit from those in the fasting group(14). However, in the obese cohort
breakfast was abolished by the increase in energy intake energy intake was not signicantly different between the
at lunch. This was not the case in our work in lean indi- breakfast and fasting groups, with those assigned break-
viduals(25), for whom total intake was greater in the fast intake consuming 14141 kJ/d (338 (95 % CI 313,
breakfast condition. Notably the breakfast provided by 988) kcal/d) more(15). This nding in obese individuals is
Astbury et al. was relatively small (about 10460 kJ consistent with the ndings of Reeves et al.(37), where the
(250 kcal)) in comparison with those provided in most difference between breakfast and fasting groups was a
other investigations (typically >16736 kJ (400 kcal)). pooled effect of lean (about 11087 kJ (265 kcal) higher)
With this in mind, it is a logical suggestion that the en- and obese individuals (about 25104 kJ (60 kcal) higher),
ergy content of larger breakfasts is less likely to be suggestive that obese individuals may compensate more
fully compensated in the next meal alone. Studies that for a morning energy decit than lean individuals under
have examined energy intake at both lunch and then din- free-living conditions. Interestingly, in our experiments
ner(28) or meals plus snacks(31) have not revealed the same obese individuals undertook both the acute in-
Proceedings of the Nutrition Society

increased intake after morning fasting, refuting the possibil- vestigation described earlier (where there was no compen-
ity that further compensation occurs throughout the day. sation observed at lunch) and the free-living assessments
This view is also supported by ndings of similar energy in- (where there was no difference in daily intake between
take during evening snacks and meals when comparing groups)(15,26). This is in contrast to the equivalent lean
morning feeding v. fasting followed by a standardised individuals who displayed limited compensation for
lunch(34). breakfast omission both inside and outside the labora-
The balance of evidence from controlled studies there- tory(14,25). The discord between these two groups of indivi-
fore suggests that breakfast omission results in some com- duals suggests either that lean and obese people respond
pensation at the next meal in lean individuals but that this differently to the study designs employed or that energy in-
next-meal effect is relatively transient with little evidence take may be more strongly inuenced by environmental
of more sustained compensatory feeding mechanisms. factors with increasing adiposity(38). For example, the en-
Interestingly, our work in obese individuals indicated simi- ergy intake compensation evident in the obese cohort may
lar energy intake at lunch independent of morning fasting be due to food choices and frequency, as opposed to the
or breakfast consumption(26). To our knowledge, this is the quantity consumed at single homogenous meals provided
rst report of ad libitum intake amongst obese adults after in an articial laboratory setting.
breakfast omission and subsequent investigations should As might be expected, the data from free-living investi-
attempt to determine if dietary compensation occurs at gations are inherently more varied than controlled labora-
later feeding occasions in this population. tory investigations and the limitations of self-reported
energy intake have recently been detailed elsewhere(39).
Intervention studies. Intervention studies attempting While these factors contribute towards systematic and ran-
to quantify the response to chronic breakfast dom error and so impact both validity and reliability, there
consumption or omission do not provide such clear is little reason to believe that comparisons between experi-
evidence as laboratory investigations for the effect of mental groups would be systematically biased by such lim-
breakfast omission upon energy intake. Early work in itations(7). Nonetheless, methods to assess diet remain
which feeding frequency was regimented throughout the challenging under free-living conditions and there are cur-
day suggested that breakfast omission leads to greater rently no viable alternatives to dietary records in some
energy intake than breakfast consumption(35). Two form if specic nutrient proles and/or feeding patterns
recent studies both from the same research group using are of interest. However, from a pure energy-balance per-
similar cross-over designs of 1-week duration provide spective, it is possible to estimate total energy intake with
further data in this regard. In the rst investigation, relative accuracy using the intake-balance method(40,41),
Halsey et al.(36) reported no difference in energy intake which exploits the energy-balance equation to derive en-
when participants either fasted or consumed an ergy entering the system as the sum of the change in energy
ad libitum high-carbohydrate breakfast under supervised storage and objectively measured energy expenditure(42).
laboratory conditions. In a subsequent investigation, The latter may itself be responsive to altered feeding pat-
participants were asked to consume a freely chosen terns and the following sections will address this possibility
breakfast within 1 h of waking for 1 week, relative to with specic reference to each individual component of en-
fasting until midday; omission of breakfast reduced daily ergy expenditure.
energy intake by 6694 kJ (160 kcal) relative to a mean
energy intake of about 1673620920 kJ (400500 kcal)
prior to midday when breakfast was consumed(37). Resting metabolic rate
Our recent investigations did not impose any dietary RMR is for a large proportion of individuals the greatest
limitations on the participants in either group other contributor to energy expenditure(43). Decreases in mass
than maintaining the morning fast until noon or adjusted RMR have been demonstrated in both

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Extended morning fasting, energy balance and health 469

starvation and hypoenergetic dieting(4446) but evidence the acute response). However, any potential effect of
for a modifying effect of chronic morning feeding pattern breakfast consumption per se on overall DIT will be
upon RMR is not apparent. Three past studies have mea- quantitatively small and inexorably outweighed by the
sured changes in RMR in response to a sustained morning energy intake required to elicit that DIT.
feeding intervention(35,47,48). Of these, Schlundt et al.(47)
demonstrated that weight loss induced by caloric restriction
in obese women resulted in similar reductions in RMR Physical activity thermogenesis
whether consuming breakfast or fasting during the morn- Of the components contributing to total energy expend-
ing. In accordance, the 2-week crossover intervention of iture, physical activity thermogenesis is undoubtedly
Farshchi et al. found no difference in RMR (or weight/ the most modiable component yet has received surpris-
body composition) following breakfast consumption or ingly little attention in the literature regarding breakfast.
skipping regimens in lean women(35). In a crossover study Higher physical activity levels assessed by questionnaire
design involving groups of lean and overweight individuals, are cross-sectionally associated with regular breakfast
1 week of breakfast consumption or fasting until noon also consumption(13,21,5557). However, this relationship has
had no effect upon RMR(48). not been explained by causal data from experimental
The results of our 6-week interventions in both lean(14) studies, with the few that are available having employed
and obese(15) individuals over 6 weeks of daily breakfast a wide variety of methodologies of varied sensitivity and
or morning fasting indicated that RMR was unaffected specicity. Several studies have investigated the effect of
Proceedings of the Nutrition Society

by morning feeding pattern (all groups stable within varying feeding frequencies upon overall energy expend-
628 kJ/d (15 kcal/d)). Therefore, the evidence uniformly iture measured using a whole body calorimeter(5860),
shows that consistently extending the overnight fast does which understandably places severe restrictions upon
not directly affect RMR beyond the predicted change natural physical activity patterns that might be respon-
associated with possible changes in body mass/ sive to breakfast outside the laboratory.
composition. Other past studies have attempted to quantify aspects
of physical activity behaviour in response to breakfast in
particular or altered daily meal frequency in general
Diet-induced thermogenesis using a variety of approaches. Physical movements
Diet-induced thermogenesis (DIT) is the smallest compo- have been estimated using hip-worn monitors, ped-
nent of energy expenditure under most circumstances and ometers or accelerometers but have failed to detect any
reects the obligatory energy expended for the processing difference in step counts during 1 week of either break-
and digestion of food. Different macronutrients induce fast or fasting(36,48) or any difference in accelerometer
varying levels of thermogenesis(49,50), but DIT is only counts when comparing a three-meal feeding pattern
ever a fraction of the energy content of the foods ingested with a single evening-meal for 8 weeks(61). However, nat-
and typically only about 10 % of intake when consuming ural adjustments in overall activity may have been
a normal mixed diet(51). Only one intervention study has masked in the latter study because participants were
examined the effect of a sustained morning feeding inter- encouraged to maintain their normal exercise through-
vention on DIT, with no effect on the thermic effect of a out the day. In addition, such measurement tools may
mixed macronutrient test drink after breakfast skipping also lack both reliability and sensitivity when applied
or consumption for 2 weeks(35). to subtle changes across all aspects of physical activity
There is some evidence that DIT is greater in the thermogenesis(62). While the issues of reliability and sen-
morning than later in the day(52,53) and the thermogenic sitivity have been overcome using doubly-labelled water
effect of breakfast is necessarily greater than morning to verify no difference in total energy expenditure be-
fasting. Indeed, when consuming breakfast and an ad tween a two- v. seven-meal daily feeding pattern(63),
libitum lunch, both lean and obese participants expend that nding is neither specic to breakfast or physical ac-
greater energy through DIT during the morning and tivity thermogenesis per se, nor does the technique reveal
afternoon than when omitting breakfast (2761 (SD temporal patterns of activity.
1381) kJ (66 (SD33) kcal) v. 2050 (SD 1213) kJ (49 (SD We employed combined heart-rate accelerometry as a
29) kcal) in lean and 2845 (SD 1255) kJ (68 (SD 33) validated tool to quantify physical activity thermogenesis
kcal) v. 1674 (SD 962) kJ (40 (SD 23) kcal) in obese; on a minute-by-minute basis under free-living conditions
Chowdhury et al., unpublished results). In studies in response to our daily breakfast v. fasting intervention.
where a xed lunch meal has been provided following This instrument is particularly sensitive to the low-
morning fasting/feeding, DIT during the afternoon was to-moderate intensity, spontaneous lifestyle activities
greater following breakfast(34) or not different relative that we hypothesised might be most responsive to break-
to fasting when measured 1 and 4 h after lunch(28). fast(9,62). Our investigation in lean individuals demon-
Where energy intake has been matched across 24 h fol- strated that daily physical activity thermogenesis was
lowing breakfast omission by increasing intake at subse- substantially greater amongst those consuming breakfast
quent meals, no difference in 24 h energy expenditure than those fasting (18493 (95% CI 1423, 35606) kJ/d
was observed(54). This suggests little modifying effect of (442 (95% CI 34, 851) kcal/d)), with a particular differ-
morning feeding pattern on DIT. Future studies should ence between groups apparent for the morning period
determine the effect of chronic breakfast omission upon and for light intensity activities(14). The obese individuals
DIT in response to feeding (i.e. a chronic adaptation in subsequently studied were less active overall and did not

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http://dx.doi.org/10.1017/S0029665116000318
470 J. A. Betts et al.

display such a difference between groups in total daily thermogenesis. Whilst both have an end result of increas-
physical activity thermogenesis (11380 (95% CI 13096, ing energy expenditure, the distinguishing factor is that
41338) kJ/d (272 (95% CI 313, 988) kcal/d)) although, the latter is dened by having a purpose. Accordingly,
like their lean counterparts, an effect on morning energy if structured exercise was already planned for as part of
expenditure was apparent (7866 (95% CI 1674, 14016) an individuals morning, then this is likely to prohibit
kJ/d (188 (95% CI 40, 335) kcal/d))(15). This suggests that the effect of breakfast consumption on physical activity
modifying feeding patterns can affect physical activity, thermogenesis, since energy expenditure is prescribed.
with the most pronounced response during the time per- The question then arises, what are the effects of breakfast
iod of energy restriction/breakfast consumption. The rea- consumption on metabolism for the morning exerciser?
sons for this are not immediately clear but might be The acute responses of exercise metabolism to prior
related to perceptions of lethargy, expectations relating feeding are well characterised. Total energy expenditure
to physical activity readiness or that reduced availability is almost entirely determined by the duration and inten-
of exogenous substrate and/or systemic metabolites may sity of the exercise bout, but substrate selection can be
limit engagement in non-essential physical exertion. drastically shifted by nutritional status. Consumption
Taken collectively, these observations that physical ac- of a mixed-macronutrient breakfast increases carbohy-
tivity levels are lower in response to fasting begin to ex- drate oxidation and suppresses fat oxidation during exer-
plain why a resolution to start skipping breakfast may cise(32,66), which is largely driven by the type and
not predict the degree of weight loss one might expect. quantity of carbohydrate in the meal(67). This is predom-
Proceedings of the Nutrition Society

The shaping of our genome prior to the agricultural revo- inantly due to the insulin-induced suppression of plasma
lution ensured that individuals evolved mechanisms to NEFA availability; insulin concentrations after a mixed-
protect against energy decit during natural fedfasted macronutrient carbohydrate-rich breakfast remain ele-
cycles on a daily basis (i.e. when almost every meal vated sufcient to all but maximally suppress palmitate
required initial investment of energy). In this sense, it appearance(68). Interestingly, the breakfast-induced sup-
might be better to express the energy-balance equation pression of fatty acid availability during exercise is not
not as Balance = Intake Expenditure but instead due to a reduction in lipolysis (at least in the subcutane-
Balance = Expenditure + Intake. The net result is un- ous adipose tissue depot) but rather to an increase in
changed but this serves as a reminder that, in terms of re-esterication(69). In addition, if the breakfast has a
survival, our investment of energy comes rst and is inev- particularly high glycaemic index, then an elevated pre-
itable, whereas food availability/procurement is uncer- exercise muscle glycogen concentration(70) can also con-
tain and may be zero. tribute to a further suppression of fat oxidation in both
Strategies designed to improve human health by target- men(71) and women(72).
ing energy balance must therefore integrate an appreci- The omission of breakfast prior to exercise (or delay-
ation of how compensatory feedback mechanisms can ing breakfast consumption until after exercise) also
operate to defend against energy decit. Conserving en- appears to have unique consequences for acute whole-
ergy via reduced physical activity can be effective in the body substrate balance. Physical exercise does not invoke
short term, but may not favour survival during a sustained the same acute energy intake response to breakfast omis-
food shortage, in which case more sedentary behaviours sion/delay presented earlier (i.e. energy intake at lunch
might be selected-out relative to the more proactive ap- and dinner is largely either unaltered(32,73,74) or does
proach of competing for what limited resources are avail- not fully compensate for breakfast omission(28)). Instead,
able early in the post-absorptive period. It therefore the increase in energy expenditure due to exercise, com-
remains a possibility that more extreme or sustained ex- bined with the shift in substrate utilisation towards greater
posure to extended daily fasting resulting in a chronically lipid oxidation with breakfast omission, results in a less
hypoenergetic diet could stimulate increased spontaneous positive (more negative) fat balance in both lean(32) and
physical activities, similar to the starvation-induced overweight men(74). This has also been observed over a
hyperactivity noted in rodents and patients with anor- full 24-h period with room calorimetry and xed energy in-
exia(64). Of course, these elegantly evolved compensatory take(75). Given the importance of endogenous carbohy-
mechanisms have become somewhat obsolete (for most) drate stores for exercise tolerance(7678), the preservation
in modern societies where food procurement is largely in- of whole-body carbohydrate balance in the presence of a
dependent of any up-front investment of energy(65). An ef- negative fat balance(32,74) could be an attractive metabolic
fective intervention today will therefore need to target milieu for the regular exerciser.
both sides of the energy-balance equation (e.g. diet and The chronic effect of breakfastexercise interactions is
physical activity); hence, the following section will con- much less clear. An emerging theme in exercise physi-
sider the arguably more natural scenario in which fasting ology is the augmentation of endurance-type training
is superimposed against a background of physical activity adaptations through manipulation of substrate availabil-
and/or exercise. ity. Methods such as multiple bouts of exercise(79,80),
reductions in dietary carbohydrate intake and timing of
dietary carbohydrate intake(81,82) all serve to reduce en-
Exercisefasting interactions dogenous or exogenous carbohydrate availability, conse-
quently elevating fatty acid availability. Whilst (to the
An important distinction should be made between phys- authors knowledge) no studies are available on the effect
ical activity thermogenesis and exercise-induced of breakfast on endurance training adaptation per se,

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http://dx.doi.org/10.1017/S0029665116000318
Extended morning fasting, energy balance and health 471

there is evidence to suggest that consumption of a However, there was an interaction effect for insulinaemic
carbohydrate-rich breakfast prior to training, in addition response to an oral glucose tolerance test in this popula-
to carbohydrate intake during every exercise training ses- tion, with a reduction in those consuming breakfast rela-
sion can impair some endurance-type training adapta- tive to an increase in those fasting. Across both groups,
tions. Specically, compared to extending the overnight the majority of health markers were unaffected by either
fast until after exercise, carbohydrate consumption before regimen. Therefore, it appears that any effects of chronic
and during exercise can attenuate and/or abolish the morning fasting upon health in healthy individuals are ei-
increases in VO2max(83) glucose tolerance, insulin sensitiv- ther non-existent or not detectable over the relatively
ity, resting muscle glycogen concentrations and GLUT4 short time period examined. Evidence for a potential ef-
content(84). It should be noted however, that these effects fect upon insulin sensitivity and glycaemic control is evi-
are not consistent across all studies of fasted-state exercise dent in the work of our group and others(14,15,35), and
training(85). tallies somewhat with reports of improved glycaemic
The energy balance and body composition responses control with greater breakfast quantity in type-2 dia-
to regular exercise training with breakfast consump- betics(90,91). However, considering that not all measures
tion/omission are currently unknown. It therefore of metabolic control demonstrated a deterioration with
remains to be seen whether the Nobel Laureate and extended morning fasting in healthy individuals, it
Exercise Physiologist A.V. Hill had a rm rationale appears that any effects are subtle at best. Future studies
for running a mile every morning prior to having could provide further insight by employing interventions
Proceedings of the Nutrition Society

breakfast (86). of longer durations, over which potential effects upon


markers of health might be more apparent.

Health outcomes
Conclusions
Much of the work examining different morning feeding
patterns as described in the present review has focused The evidence reviewed suggests that breakfast omission
on components of energy balance. Considering the sever- affects some components of energy balance much more
ity of the growing issue of obesity(87) and the general pre- than others. There is no evidence to suggest that breakfast
occupation of the public/media with the effects of diet consumption per se affects RMR, or DIT of subsequent
upon weight, this is not surprising. However, it is import- meals or over the day as a whole. Evidence that breakfast
ant to keep in mind that the primary reason for the study of affects energy intake is compelling for laboratory studies,
energy balance is not as an endpoint in itself, but because with the majority of studies showing energetic compensa-
of our interest in the potential impact of an individuals en- tion at the next meal, but not sufcient to eliminate the
ergy (im)balance upon factors that may then affect their decit from morning fasting. In addition, designs where
health. While chronic energy (im)balance is potentially afternoon/evening feeding has been allowed do not dem-
an important contributor to negative health outcomes, onstrate sustained compensation for breakfast omission.
specic components of energy balance such as physical Experiments outside the laboratory understandably pro-
activity can also impact disease and mortality risk inde- duce more varied results, with the balance of evidence sug-
pendent of net energy surplus/decit or changes in adipos- gesting that energy intake is either lower or similar when
ity(88,89). Therefore, it is perfectly plausible that the omitting breakfast. Our work in lean and obese groups
omission/consumption of breakfast might affect markers would suggest that there are differences between groups
of health independent of energy balance. in energy intake responses based on adiposity. The body
While there is a wealth of evidence for increased dis- of evidence taken together supports the concept that, in
ease risk in those that omit breakfast(14), randomised general, energy intake is reduced when breakfast is omit-
controlled trials that have provided causal mechanisms ted, with limited support for the popular perception of
to explain these observations remain very limited. In greater overall energy intake after breakfast omission.
the two prior studies where health markers have been While much work has investigated energy intake in re-
measured, Stote et al.(61) report increased lipoproteins sponse to breakfast omission, there is a severe lack of
relative to a three-meal pattern (total, HDL and LDL) studies investigating the most modiable component of
when individuals adhered to a one-meal a day regimen. energy expenditure-physical activity energy expenditure,
In a less extreme model, Farshchi et al.(35) report when with some studies limited by measurement issues. Our
delaying morning intake until 10.30 hours each morning work in both lean and obese individuals suggests that
for 2 weeks that total and LDL-cholesterol and insulin breakfast omission may lower physical activity energy ex-
response to a test drink increased (although other mea- penditure, particularly during the morning, although this
sures of insulin sensitivity remained unchanged), relative needs conrmation and the potential reasons for this
to a reduction when consuming breakfast daily. Our re- phenomenon remain to be established. The majority of
cent studies have extended this evidence by measuring studies conducted to date have been of relatively short
several markers related to CVD risk and metabolic con- duration, but those that have examined the effect of
trol. In lean individuals, only a modest increase in glu- breakfast omission upon body weight do not support
cose variability in those fasting during the afternoon/ the strongly established public perceptions and correl-
evening was detected(14), with no effects for 24 h gly- ational evidence that omission of breakfast is associated
caemic control detected in obese individuals(15). with weight-gain.

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http://dx.doi.org/10.1017/S0029665116000318
472 J. A. Betts et al.

Future investigations should focus on concurrently 4. Odegaard AO, Jacobs DR Jr, Steffen LM et al. (2013)
measuring all aspects of energy balance, to provide a ful- Breakfast frequency and development of metabolic risk.
ler understanding of the effects of breakfast omission Diab Care 36, 31003106.
upon individual components (and importantly the inter- 5. ONeil CE, Byrd-Bredbenner C, Hayes D et al. (2014) The
role of breakfast in health: denition and criteria for a qual-
action of these components). Longer-term studies are
ity breakfast. J Acad Nutr Diet 114, Suppl. 12, S8S26.
needed to conclusively establish the effects of breakfast 6. Berry MK, Russo A, Wishart JM et al. (2002) Effect of
omission upon health markers, with more studies solid meal on gastric emptying of, and glycemic and cardio-
required examining overweight and obese populations. vascular responses to, liquid glucose in older subjects. Am J
Breakfast may or may not be the most important meal Physiol 284, G655G662.
of the day, but it is certainly an important meal to inves- 7. de Castro JM (1994) Accommodation of particular foods
tigate further. or beverages into spontaneously ingested evening meals.
Appetite 23, 5766.
8. Ruge T, Hodson L, Cheeseman J et al. (2009) Fasted to fed
trafcking of Fatty acids in human adipose tissue reveals a
Acknowledgements novel regulatory step for enhanced fat storage. J Clin
Endocrinol Metab 94, 17811788.
The authors thank those who participated in the trial for
9. Betts JA, Thompson D, Richardson JD et al. (2011) Bath
their time and commitment. Breakfast Project (BBP) Examining the role of extended
Proceedings of the Nutrition Society

daily fasting in human energy balance and associated


health outcomes: study protocol for a randomised con-
Financial Support trolled trial [ISRCTN31521726]. Trials 12, 172.
10. Wright DA, Sherman A & Dernbach AR (1991)
Carbohydrate feedings before, during, or in combination
This research was funded by a grant from the improve cycling performance. J Appl Physiol 71, 1082
Biotechnology and Biological Sciences Research 1088.
Council (BBSRC; BB/H008322/1) and is registered at 11. Brown AW, Bohan Brown MM & Allison DB (2013) Belief
www.isrctn.org (ISRCTN31521726). beyond the evidence: using the proposed effect of breakfast
on obesity to show 2 practices that distort scientic evi-
dence. Am J Clin Nutr 98, 12981308.
12. Batterham AM & Atkinson G (2005) How big does my
Conicts of Interest sample size need to be? A primer on the murky world of
sample size estimation. Phys Ther Sport 6, 153163.
None. 13. Dhurandhar EJ, Dawson J, Alcorn A et al. (2014) The ef-
fectiveness of breakfast recommendations on weight loss: a
randomized controlled trial. Am J Clin Nutr 100, 507513.
14. Betts JA, Richardson JD, Chowdhury EA et al. (2014) The
Authorship causal role of breakfast in energy balance and health: a ran-
domized controlled trial in lean adults. Am J Clin Nutr 100,
J. A. B. has provided consultancy for PepsiCo, Lucozade 539547.
Ribena Suntory and Kellogg, J. T. G. has provided con- 15. Chowdhury EA, Richardson JD, Holman GD et al. (2016)
sultancy for PepsiCo, Lucozade Ribena Suntory and The causal role of breakfast in energy balance and health: a
FrieslandCampina. J. A. B., K. T. and D. T. designed randomized controlled trial in obese adults. Am J Clin Nutr
the research; J. A. B., J. D. R., E. A. C. and 103, 747756.
D. T. conducted the research; K. T. provided essential 16. Cho S, Dietrich M, Brown CJ et al. (2003) The effect of
reagents and materials; J. A. B., E. A. C. and J. D. R. breakfast type on total daily energy intake and body
analysed the data and performed statistical analysis; mass index: results from the Third National Health and
Nutrition Examination Survey (NHANES III). J Am Coll
E. A. C., J. A. B. and J. T. G. co-wrote the paper and
Nutr 22, 296302.
have primary responsibility for nal content. All authors 17. Deshmukh-Taskar PR, Nicklas TA, ONeil CE et al.
read, edited and approved of the nal manuscript. (2010) The relationship of breakfast skipping and type of
breakfast consumption with nutrient intake and weight sta-
tus in children and adolescents: the National Health and
Nutrition Examination Survey 19992006. J Am Diet
References
Assoc 110, 869878.
1. Cahill LE, Chiuve SE, Mekary RA et al. (2013) Prospective 18. Nicklas TA, Myers L, Reger C et al. (1998) Impact of
study of breakfast eating and incident coronary heart dis- breakfast consumption on nutritional adequacy of the
ease in a cohort of male US health professionals. diets of young adults in Bogalusa, Louisiana: ethnic and
Circulation 128, 337343. gender contrasts. J Am Diet Assoc 98, 14321438.
2. Mekary RA, Giovannucci E, Cahill L et al. (2013) Eating 19. Nicklas TA, ONeil CE & Berenson GS (1998) Nutrient
patterns and type 2 diabetes risk in older women: breakfast contribution of breakfast, secular trends, and the role of
consumption and eating frequency. Am J Clin Nutr 98, ready-to-eat cereals: a review of data from the Bogalusa
436443. Heart Study. Am J Clin Nutr 67, 757S763S.
3. Mekary RA, Giovannucci E, Willett WC et al. (2012) 20. Kant AK & Graubard BI (2015) Within-person compari-
Eating patterns and type 2 diabetes risk in men: breakfast son of eating behaviors, time of eating, and dietary intake
omission, eating frequency, and snacking. Am J Clin Nutr on days with and without breakfast: NHANES 2005
95, 11821189. 2010. Am J Clin Nutr 102, 661670.

Downloaded from http:/www.cambridge.org/core. IP address: 80.82.78.170, on 12 Dec 2016 at 03:38:05, subject to the Cambridge Core terms of use, available at http:/www.cambridge.org/core/terms.
http://dx.doi.org/10.1017/S0029665116000318
Extended morning fasting, energy balance and health 473

21. Wyatt HR, Grunwald GK, Mosca CL et al. (2002) 40. Gilmore LA, Ravussin E, Bray GA et al. (2014) An object-
Long-term weight loss and breakfast in subjects in the ive estimate of energy intake during weight gain using the
National Weight Control Registry. Obes Res 10, 7882. intake-balance method. Am J Clin Nutr 100, 806812.
22. Blundell J, de Graaf C, Hulshof T et al. (2010) Appetite 41. de Jonge L, DeLany JP, Nguyen T et al. (2007) Validation
control: methodological aspects of the evaluation of study of energy expenditure and intake during calorie re-
foods. Obes Rev 11, 251270. striction using doubly labeled water and changes in body
23. Karra E & Batterham RL (2010) The role of gut hormones composition. Am J Clin Nutr 85, 7379.
in the regulation of body weight and energy homeostasis. 42. Racette SB, Das SK, Bhapkar M et al. (2012) Approaches
Mol Cell Endocrinol 316, 120128. for quantifying energy intake and %calorie restriction dur-
24. Cummings DE, Frayo RS, Marmonier C et al. (2004) ing calorie restriction interventions in humans: the multi-
Plasma ghrelin levels and hunger scores in humans initiat- center CALERIE study. Am J Physiol Endocrinol Metab
ing meals voluntarily without time- and food-related cues. 302, E441E448.
Am J Physiol Endocrinol Metab 287, E297E304. 43. Carpenter WH, Poehlman ET, OConnell M et al. (1995)
25. Chowdhury EA, Richardson JD, Tsintzas K et al. Inuence of body composition and resting metabolic rate
(2015) Carbohydrate-rich breakfast attenuates glycaemic, on variation in total energy expenditure: a meta-analysis.
insulinaemic and ghrelin response to ad libitum lunch rela- Am J Clin Nutr 61, 410.
tive to morning fasting in lean adults. Br J Nutr 114, 44. Doucet E, St-Pierre S, Almeras N et al. (2001) Evidence for
98107. the existence of adaptive thermogenesis during weight loss.
26. Chowdhury EA, Richardson JD, Tsintzas K et al. (2016) Br J Nutr 85, 715723.
Proceedings of the Nutrition Society

Effect of extended morning fasting upon ad libitum lunch 45. Dulloo AG & Jacquet J (1998) Adaptive reduction in basal
intake and associated metabolic and hormonal responses metabolic rate in response to food deprivation in humans: a
on obese adults. Int J Obes, 40, 305311. role for feedback signals from fat stores. Am J Clin Nutr 68,
27. Clayton DJ & James LJ (2015) The effect of breakfast on 599606.
appetite regulation, energy balance and exercise perform- 46. Martin CK, Heilbronn LK, de Jonge L et al. (2007) Effect
ance. Proc Nutr Soc 19. of calorie restriction on resting metabolic rate and spontan-
28. Clayton DJ, Barutcu A, Machin C et al. (2015) Effect of eous physical activity. Obesity 15, 29642973.
breakfast omission on energy intake and evening exercise 47. Schlundt DG, Hill JO, Sbrocco T et al. (1992) The role of
performance. Med Sci Sports Exerc 47, 26452652. breakfast in the treatment of obesity: a randomized clinical
29. Hamman L & Hirschmann II (1919) Studies on blood sugar; trial. Am J Clin Nutr 55, 645651.
IV. Effects upon the blood sugar of the repeated ingestion of 48. Reeves S, Huber JW, Halsey LG et al. (2015) A cross-over
glucose. Johns Hopkins Hospital Bulletin 30, 306307. experiment to investigate possible mechanisms for lower
30. Berthoud HR & Morrison C (2008) The brain, appetite, BMIs in people who habitually eat breakfast. Eur J Clin
and obesity. Annu Rev Psychol 59, 5592. Nutr 69, 632637.
31. Levitsky DA & Pacanowski CR (2013) Effect of skipping 49. Tappy L (1996) Thermic effect of food and sympathetic
breakfast on subsequent energy intake. Physiol Behav nervous system activity in humans. Reprod Nutr Dev 36,
119, 916. 391397.
32. Gonzalez JT, Veasey RC, Rumbold PL et al. (2013) 50. Westerterp KR, Wilson SA & Rolland V (1999) Diet
Breakfast and exercise contingently affect postprandial induced thermogenesis measured over 24 h in a respiration
metabolism and energy balance in physically active chamber: effect of diet composition. Int J Obes Relat
males. Br J Nutr 110, 721732. Metab Disord 23, 287292.
33. Astbury NM, Taylor MA & Macdonald IA (2011) 51. Westerterp KR (2004) Diet induced thermogenesis. Nutr
Breakfast consumption affects appetite, energy intake, Metab (Lond) 1, 5.
and the metabolic and endocrine responses to foods con- 52. Bo S, Fadda M, Castiglione A et al. (2015) Is the timing of
sumed later in the day in male habitual breakfast eaters. caloric intake associated with variation in diet-induced
J Nutr 141, 13811389. thermogenesis and in the metabolic pattern? A randomized
34. Thomas EA, Higgins J, Bessesen DH et al. (2015) Usual cross-over study. Int J Obes (Lond) 39, 16891695.
breakfast eating habits affect response to breakfast skip- 53. Romon M, Edme JL, Boulenguez C et al. (1993) Circadian
ping in overweight women. Obesity 23, 750759. variation of diet-induced thermogenesis. Am J Clin Nutr
35. Farshchi HR, Taylor MA & Macdonald IA (2005) 57, 476480.
Deleterious effects of omitting breakfast on insulin sensitiv- 54. Kobayashi F, Ogata H, Omi N et al. (2014) Effect of
ity and fasting lipid proles in healthy lean women. Am J breakfast skipping on diurnal variation of energy metabol-
Clin Nutr 81, 388396. ism and blood glucose. Obes Res Clin Pract 8, e201e298.
36. Halsey LG, Huber JW, Low T et al. (2011) Does consum- 55. Smith KJ, McNaughton SA, Cleland VJ et al. (2013)
ing breakfast inuence activity levels? An experiment into Health, behavioral, cognitive, and social correlates of
the effect of breakfast consumption on eating habits and breakfast skipping among women living in socioeconomic-
energy expenditure. Publ Health Nutr, 18. ally disadvantaged neighborhoods. J Nutr 143, 17741784.
37. Reeves S, Huber JW, Halsey LG et al. (2014) Experimental 56. van der Heijden AA, Hu FB, Rimm EB et al. (2007) A pro-
manipulation of breakfast in normal and overweight/obese spective study of breakfast consumption and weight gain
participants is associated with changes to nutrient and en- among U.S. men. Obesity 15, 24632469.
ergy intake consumption patterns. Physiol Behav 133, 57. Barr SI, DiFrancesco L & Fulgoni VL III (2013)
130135. Consumption of breakfast and the type of breakfast con-
38. Mela DJ (2006) Eating for pleasure or just wanting to eat? sumed are positively associated with nutrient intakes and
Reconsidering sensory hedonic responses as a driver of adequacy of Canadian adults. J Nutr 143, 8692.
obesity. Appetite 47, 1017. 58. Smeets AJ & Westerterp-Plantenga MS (2008) Acute
39. Dhurandhar NV, Schoeller D, Brown AW et al. (2015) effects on metabolism and appetite prole of one meal dif-
Energy balance measurement: when something is not better ference in the lower range of meal frequency. Br J Nutr 99,
than nothing. Int J Obes (Lond) 39, 11091113. 13161321.

Downloaded from http:/www.cambridge.org/core. IP address: 80.82.78.170, on 12 Dec 2016 at 03:38:05, subject to the Cambridge Core terms of use, available at http:/www.cambridge.org/core/terms.
http://dx.doi.org/10.1017/S0029665116000318
474 J. A. Betts et al.

59. Dallosso HM, Murgatroyd PR & James WP (1982) 76. Bergstrom J, Hermansen L, Hultman E et al. (1967) Diet,
Feeding frequency and energy balance in adult males. muscle glycogen and physical performance. Acta Physiol
Hum Nutr Clin Nutr 36C, 2539. Scand 71, 140150.
60. Taylor MA & Garrow JS (2001) Compared with nibbling, 77. Alghannam AF, Jedrzejewski D, Tweddle MG et al. (2016)
neither gorging nor a morning fast affect short-term energy Impact of muscle glycogen availability on the capacity for
balance in obese patients in a chamber calorimeter. Int J repeated exercise in man. Med Sci Sports Exerc 48,
Obes Relat Metab Disord 25, 519528. 123131.
61. Stote KS, Baer DJ, Spears K et al. (2007) A controlled trial 78. Casey A, Short AH, Hultman E et al. (1995) Glycogen
of reduced meal frequency without caloric restriction in resynthesis in human muscle bre types following
healthy, normal-weight, middle-aged adults. Am J Clin exercise-induced glycogen depletion. J Physiol (Lond)
Nutr 85, 981988. 483, 265271.
62. Thompson D, Batterham AM, Bock S et al. (2006) 79. Hansen AK, Fischer CP, Plomgaard P et al. (2005) Skeletal
Assessment of low-to-moderate intensity physical activity muscle adaptation: training twice every second day vs.
thermogenesis in young adults using synchronized heart training once daily. J Appl Physiol (1985) 98, 9399.
rate and accelerometry with branched-equation modeling. 80. Yeo WK, McGee SL, Carey AL et al. (2010) Acute signal-
J Nutr 136, 10371042. ling responses to intense endurance training commenced
63. Verboeket-van de Venne WP, Westerterp KR & Kester AD with low or normal muscle glycogen. Exp Physiol 95,
(1993) Effect of the pattern of food intake on human en- 351358.
ergy metabolism. Br J Nutr 70, 103115. 81. Marquet LA, Brisswalter J, Louis J et al. (2016) Enhanced
Proceedings of the Nutrition Society

64. Hebebrand J, Exner C, Hebebrand K et al. (2003) endurance performance by periodization of CHO
Hyperactivity in patients with anorexia nervosa and in Intake: sleep low strategy. Med Sci Sport Exerc 48,
semistarved rats: evidence for a pivotal role of hypoleptine- 663672.
mia. Physiol Behav 79, 2537. 82. Van Proeyen K, Szlufcik K, Nielens H et al. (2011)
65. Eaton SB & Eaton SB (2003) An evolutionary perspective Benecial metabolic adaptations due to endurance exercise
on human physical activity: implications for health. Comp training in the fasted state. J Appl Physiol (1985) 110,
Biochem Physiol 136, 153159. 236245.
66. Wu CL & Williams C (2006) A low glycemic index meal 83. Stannard SR, Buckley AJ, Edge JA et al. (2010)
before exercise improves endurance running capacity in Adaptations to skeletal muscle with endurance exercise
men. Int J Sport Nutr Exerc Metab 16, 510527. training in the acutely fed versus overnight-fasted state.
67. Wu CL, Nicholas C, Williams C et al. (2003) The inuence J Sci Med Sport 13, 465469.
of high-carbohydrate meals with different glycaemic indices 84. Van Proeyen K, Szlufcik K, Nielens H et al. (2010)
on substrate utilisation during subsequent exercise. Br J Training in the fasted state improves glucose tolerance dur-
Nutr 90, 10491056. ing fat-rich diet. J Physiol 588, Pt 21, 42894302.
68. Jensen MD, Caruso M, Heiling V et al. (1989) Insulin regu- 85. De Bock K, Derave W, Eijnde BO et al. (2008) Effect of
lation of lipolysis in nondiabetic and IDDM subjects. training in the fasted state on metabolic responses during
Diabetes 38, 15951601. exercise with carbohydrate intake. J Appl Physiol (1985)
69. Enevoldsen LH, Simonsen L, Macdonald IA et al. (2004) 104, 10451055.
The combined effects of exercise and food intake on adi- 86. Hill AV & Lupton H (1923) Muscular exercise, lactic acid,
pose tissue and splanchnic metabolism. J Physiol 561, Pt and the supply and utilization of oxygen. Q J Med 16, 135
3, 871882. 171.
70. Wee SL, Williams C, Tsintzas K et al. (2005) Ingestion of a 87. Wang YC, McPherson K, Marsh T et al. (2011) Health and
high-glycemic index meal increases muscle glycogen stor- economic burden of the projected obesity trends in the
age at rest but augments its utilization during subsequent USA and the UK. Lancet 378, 815825.
exercise. J Appl Physiol 99, 707714. 88. Ekelund U, Ward HA, Norat T et al. (2015) Physical activ-
71. Wee SL, Williams C, Gray S et al. (1999) Inuence of high ity and all-cause mortality across levels of overall and ab-
and low glycaemic index meals on endurance running cap- dominal adiposity in European men and women: the
acity. Med Sci Sport Exerc 31, 393399. European Prospective Investigation into Cancer and
72. Stevenson E, Williams C, Nute M et al. (2008) Inuence of Nutrition Study (EPIC). Am J Clin Nutr 101, 613621.
the glycaemic index of an evening meal on substrate oxida- 89. Walhin JP, Richardson JD, Betts JA, et al. (2013)
tion following breakfast and during exercise the next day in Exercise counteracts the effects of short-term overfeeding
healthy women. Eur J Clin Nutr 62, 608616. and reduced physical activity independent of energy imbal-
73. Deighton K, Zahra JC & Stensel DJ (2012) Appetite, en- ance in healthy young men. J Physiol 591, Pt 24,
ergy intake and resting metabolic responses to 60 min 62316243.
treadmill running performed in a fasted versus a postpran- 90. Jakubowicz D, Wainstein J, Ahren B, et al. (2015) Fasting
dial state. Appetite 58, 946954. until noon triggers increased postprandial hyperglycemia
74. Farah NM & Gill JM (2013) Effects of exercise before or and impaired insulin response after lunch and dinner in
after meal ingestion on fat balance and postprandial me- individuals with type 2 diabetes: a randomized clinical
tabolism in overweight men. Br J Nutr 109, 22972307. trial. Diabetes Care 38, 18201826.
75. Shimada K, Yamamoto Y, Iwayama K et al. (2013) Effects 91. Rabinovitz HR, Boaz M, Ganz T et al. (2014) Big break-
of post-absorptive and postprandial exercise on 24 h fat fast rich in protein and fat improves glycemic control in
oxidation. Metabolism 62, 793800. type 2 diabetics. Obesity 22, E46E54.

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