Exercise, Appetite and Weight Control

18 Pages·2016·0.93 MB·English

nutrients
Review
Exercise, Appetite and Weight Control: Are There
Differences between Men and Women?
AliceE.Thackray1,KevinDeighton2,JamesA.King1andDavidJ.Stensel1,*
1 SchoolofSport,ExerciseandHealthSciences,LoughboroughUniversity,LeicestershireLE113TU,UK;
[email protected](A.E.T.);[email protected](J.A.K.)
2 InstituteforSport,PhysicalActivityandLeisure,LeedsBeckettUniversity,LeedsLS63QS,UK;
[email protected]
* Correspondence:[email protected];Tel.:[phone]
Received:25August2016;Accepted:18September2016;Published:21September2016
Abstract:Recentyearshavewitnessedsignificantresearchinterestsurroundingtheinteractionamong
exercise,appetiteandenergybalance,whichhasimportantimplicationsforhealth. Themajorityof
exerciseandappetiteregulationstudieshavebeenconductedinmales. Consequently,opportunities
toexaminesex-baseddifferenceshavebeenlimited,butrepresentaninterestingavenueofinquiry
consideringpostulationsthatmenexperiencegreaterweightlossafterexerciseinterventionsthan
women. Thisarticlereviewsthescientificliteraturerelatingtotheacuteandchroniceffectsofexercise
on appetite control in men and women. The consensus of evidence demonstrates that appetite,
appetite-regulatoryhormoneandenergyintakeresponsestoacuteexercisedonotdifferbetween
thesexes, andthereislittleevidenceindicatingcompensatorychangesoccurafteracuteexercise
ineithersex. Limitedevidencesuggestswomenrespondtotheinitiationofexercisetrainingwith
more robust compensatory alterations in appetite-regulatory hormones than men, but whether
this translates to long-term differences is unknown. Current exercise training investigations do
notsupportsex-baseddifferencesinappetiteorobjectivelyassessedenergyintake,andincreasing
exerciseenergyexpenditureelicitsatmostapartialenergyintakecompensationinbothsexes. Future
well-controlledacuteandchronicexercisestudiesdirectlycomparingmenandwomenarerequired
toexpandthisevidencebase.
Keywords: appetite;appetite-regulatoryhormones;compensation;energybalance;energyintake;
exercise;sex-baseddifferences;weightcontrol
1. Introduction
Obesityisamajorriskfactorforseveralchronicdiseases,includingtype2diabetesmellitusand
cardiovasculardisease,andremainsasignificantglobalburdenfromapublichealthandeconomic
standpoint[1,2]. Weightlossaslittleas3%ofinitialbodymassissufficienttopromotefavourable
changes in several chronic disease risk markers and can be accomplished by increasing energy
expenditurethroughexerciseand/orreducingenergyintaketoachieveasustainednegativeenergy
balance [3]. Recent years have witnessed significant research interest surrounding the interaction
betweenexercise,appetiteandenergybalance,whichhasdirectimplicationsfortheimplementation
ofexerciseasaweightmanagementstrategy[4].
Similartomanyscientificfields,themajorityofexerciseandappetiteregulationstudieshave
traditionallyfocusedresearcheffortsonmen. Consequently,muchlessisknownabouttheinteraction
between exercise and appetite in women, and the opportunity to examine potential sex-based
differences has been limited. A handful of exercise training studies have demonstrated that men
experience greater reductions in body mass and body fat than women [5–7], although this is not
auniversalfinding[8,9]. Authorssupportingtheconceptofdivergentweightlossoutcomeshave
Nutrients2016,8,583;doi:10.3390/nu8090583 www.mdpi.com/journal/nutrients
Nutrients2016,8,583 2of18
suggestedthatwomendemonstrategreatercompensatoryresponsestoexercisebymoreaccurately
balancingenergyintakeandexpenditureinordertodefendbodyfatstoresandpreservereproductive
function[10–12].
Exercise-inducedchangesinhormonesimplicatedinappetitecontrolandenergybalance(e.g.,
acylated ghrelin, peptide YY (PYY), glucagon-like peptide-1 (GLP-1), insulin, and leptin) may
contributetosex-baseddifferencesinbodyfatlossafterexercise[13]. Althoughbasedonalimited
numberofstudies,apreviousreviewconcludedthatwomenexhibitcompensatorychangesinappetite
ratings and hormones conducive to appetite stimulation; a response that is not seen in men [11].
However,thisconclusionhasnotbeensupportedbymorerecentexperimentalstudies,whichhave
documentedsimilarappetite,appetite-regulatoryhormoneandenergyintakeresponsestoacuteand
chronicexercise-inducedenergydeficitsinmenandwomen[8,14,15].
The purpose of this article is to review recent developments regarding appetite,
appetite-regulatoryhormoneandenergyintakeresponsestosingleboutsofexercise(acuteresponses)
andexercisetraining(chronicresponses)inmenandwomen. Furthermore,thisreviewwillconsider
thepotentialimplicationsofthesefindingsforhealthandhighlightimportantareasforfutureresearch.
2. Appetite-RegulatoryHormones
Appetiteandenergyintakeareregulatedatthephysiologicallevelbytheneuroendocrinesystem,
which involves complex interactions between central and peripheral mediated pathways [16,17].
Appetite-regulatoryhormonesincludeepisodicgutsignalsthataresensitivetoshort-termfluctuations
infeedingbehaviourandcontrolhungerandsatietyonameal-to-mealbasis(e.g.,acylatedghrelin,
PYY,andGLP-1),andtonichormonalsignalsthatregulatelong-termchangesinenergybalanceand
bodyfat(e.g.,insulin,andleptin). Abriefintroductiontothesehormonesispresentedhere,butthe
interestedreaderisdirectedtoanumberofcomprehensivereviewsdocumentingthepreciseroleof
thesehormonesinthehomeostaticregulationofappetiteandenergybalance[16–19].
Oftheshort-actingappetiteregulatorysignals,ghrelinisuniqueastheonlyknowngutpeptide
that is orexigenic, and is predominantly secreted into the circulation by the oxyntic glands of the
stomach. Ghrelin exists in the circulation in two forms (acylated and unacylated) and, although
only10%–20%ofcirculatingghrelinisacylatedghrelin,thisformisbelievedtobesolelyresponsible
forappetitestimulation[20]. Circulatingghrelinconcentrationsincreasepreprandiallyandarerapidly
suppressedpostprandiallyonameal-to-mealbasis. Thistemporalpatternoffluctuationisindicative
ofanimportantroleincoordinatingmealinitiation[21].
Workinginoppositiontoghrelin,onameal-to-mealbasis,severalappetite-inhibitinghormones
serve to promote post-meal satiation and satiety (e.g., PYY, GLP-1, cholecystokinin, pancreatic
polypeptide,andamylin). Ofprimaryrelevancetothisreview,PYYispredominantlysynthesisedand
secretedfromtheintestinalL-cellsandispresentperipherallyintwoforms(PYY andPYY ),
1–36 3–36
withPYY representingthemostabundantandbiologicallyactiveform. ConcentrationsofPYY
3–36
arelowinthefastedstateandincreaserapidlyaftermealintake,whichhighlightsapotentialrolein
mealterminationandsensationsoffullnessbetweenmeals. Glucagon-likepeptide-1isalsosecreted
fromtheintestinalL-cellsinresponsetonutrientintakeandsimilarlycontributestomealtermination
andsatiety. Itexistsasanactive(GLP )andinactive(GLP )form,withtheactiveformrapidly
7–36 9–37
degradedtoitsinactiveformuponsecretionintothecirculation. Theappetite-inhibitingeffectofthese
hormonesisfurthersupportedbystudiesdemonstratingthatperipheraladministrationofPYY [22]
3–36
andGLP-1[23]stimulatessatietyandreducesadlibitumfoodintakeinleanandobeseindividuals.
Leptin,secretedprimarilyfromadipocytes,andinsulin,releasedbythebetacellsofthepancreas,
are important regulators of energy balance, which are implicated in the long-term control of food
intake and energy expenditure. Leptin and insulin are secreted in concentrations proportional to
bodyfatmass,andactdirectlyonthehypothalamusandotherbrainregionstoexertanorexigenic
effects. Circulatingleptinandinsulinconcentrationsareelevatedinobeseindividuals,suggestingthat
adegreeofresistancetotheanorexigeniceffectsofthesehormonesmayoccurwithobesity. Thisis
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furthersupportedbyevidencethattheaccumulationofadiposetissueweakenstheinhibitoryeffectof
fatmassonenergyintake[24,25].
3. ExerciseandWeightLoss
Exerciseisanimportantcomponentofweightmanagement[3],andpromotesamyriadofhealth
benefits independent of weight loss [26]. It is well documented that exercise typically results in
modestweightlossthatcanbeenhancedwhenexerciseiscombinedwithdietarymodifications[27,28].
However,theefficacyofexerciseasasuccessfulstrategyforweightmanagementvariesmarkedly
between individuals [29]. Interestingly, it has been suggested that sex may be a primary factor
that affects the ability of structured exercise to promote weight loss and/or facilitate weight
management[30].
The strongest evidence of a sex-based difference in the weight loss response to exercise was
providedintheMidwestExerciseTrialbyDonnellyandcolleagues[6].Thisstudyinvolveda16-month
supervisedexercisetrainingprogramatasetintensityandduration(fivedaysperweek,20–45min
.
persessionat55%–70%peakoxygenuptake(VO ))withadlibitumdietinpreviouslysedentary
2peak
men and women. After the exercise intervention, men lost an average of 5.2 kg in body weight
and4.9kginfatmass,whereaswomenmaintainedbodyweightandfatmass. Otherstudieshave
alsodemonstratedthatmenexperiencegreaterweightlossthanwomeninresponsetoasupervised
programofexercisewhenexerciseisprescribedatasimilardurationandrelativeexerciseintensity
acrossthesexes[5,31,32].
However,inmanyofthesestudies,theexercise-inducedenergyexpenditurewassubstantially
greater in men than women. This has been suggested as a potential reason for the reported
sex-based differences in exercise-induced weight loss [33], in accordance with evidence that the
energyexpenditureofexerciseisthestrongestpredictoroffatlossduringanexerciseprogram[34,35].
Exercisetrainingstudiesprescribingexercisebasedonenergyexpenditurehavereportedcomparable
bodycompositionchangesinresponsetothetrainingstimulusinmenandwomen[8,9,36].Specifically,
Donnellyandcolleagues[9]havepublishedfindingsfromasubsequentrandomisedcontrolledtrial
asafollow-uptotheMidwestExerciseTrialinwhichtheexercise-inducedenergyexpenditurewas
matchedbetweenmenandwomenovera10-monthsupervisedaerobicexercisetrainingintervention.
Incontrasttotheirearlierstudy[6],whentheenergyexpenditurewasequivalentbetweenthesexes,
similarreductionsinbodyweightandbodyfatwereseenbetweenmenandwomen[9].
Acommonfindingintheliteratureisthedegreeofindividualvariationintheweightlossresponse
toexercisetraininginbothsexes[8,9,29,35,37,38]. Ithasbeensuggestedthatindividualdifferences
in compensatory behaviours that negate the exercise-induced energy deficit may be responsible
for this variability [29]. Specifically, evidence of increased hunger and energy intake have been
reportedinindividualswhoexperiencealowerthanexpectedweightlossafteraperiodofexercise
training[29,37,38]. Consequently,studiesinvestigatingtheeffectofexerciseonappetiteregulation
(appetiteperceptions,appetite-regulatoryhormones,energyintake)inmenandwomenareimportant
andwillbediscussedinthefollowingsectionsofthisreview.
4. AcuteEffectsofExerciseonAppetite,Appetite-RegulatoryHormonesandEnergyIntake
Aplethoraofstudieshavebeenconductedexaminingtheappetite,appetite-regulatoryhormone
andenergyintakeresponsestoacuteexerciseinmen,andtoamuchlesserextent,women.Thisresearch
hasbeenreviewedindetailelsewhere[4,39–43],butabriefsynopsisofthemostpertinentstudiesis
presentedinthisarticletoframetheresearchliteraturewhichhasexaminedsex-baseddifferences.
4.1. AppetiteandAppetite-RegulatoryHormones
The consensus of evidence in healthy, normal weight men suggests that acylated ghrelin
concentrationsaretransientlysuppressed,andsatietyhormones,mostnotablyPYYandGLP-1,are
elevated during and immediately after an acute bout of exercise. Such hormonal changes often
Nutrients2016,8,583 4of18
coincide with a transient reduction in subjective appetite responses, which has been described
as “exercise-induced anorexia” [44]. These responses become apparent when acute exercise is
.
performed≥60%ofVO typically[45–49],andhavebeenreplicatedduringavarietyofexercise
2peak
modesincludingrunning[45,46,48],cycling[47,50–53],swimming[54],resistanceexercise[46,55]and
high-intensity interval exercise [52,53,56]. Circulating appetite-regulatory hormones and appetite
ratingstypicallyreturntocontrolvalueswithin30to60minofexercisecompletion[39,46,48];however,
compensatory increases in appetite have been reported in some studies [52,54,57]. Furthermore,
currentevidencesuggeststhatacuteexerciseelicitssimilarappetiteandappetite-regulatoryhormone
responsesinleanandoverweightmen[47],anddoesnotstimulatecompensatorychangesinthose
whoareoverweightorobese[47,58].
Despitepostulationsthatsex-baseddifferencesinappetiteregulationmayexisttoenablewomen
to preserve energy balance and reproductive function [10–12], several acute studies conducted in
womensuggestthattheyrespondsimilarlytomen. Specifically,transientalterationsinappetiteand
appetite-regulatoryhormoneconcentrations(acylatedghrelin,PYY ,andGLP-1)havebeenreported
3–36
inadirectionexpectedtosuppressappetiteinhealthy,recreationallyactive[15],endurance-trained[59]
andoverweightandobese[60]women. Furthermore,themajorityofstudiesreportnoevidenceof
compensatoryincreasesinappetiteperceptionsandappetite-regulatoryhormonesupto7.5haftera
singleboutofexerciseinwomen[15,59–62].
However, exceptions have been observed in the literature with some studies demonstrating
that women do not exhibit an acute exercise-induced suppression of appetite [62–64] or changes
in appetite-regulatory hormones [61,62]. Furthermore, in contrast to the aforementioned studies
in men and women, Larson-Meyer and colleagues [64] reported an increase in acylated ghrelin
.
concentrationsduringthe2hperiodafter60minrunningat70%VO . Suchdiscrepanciesare
2peak
likely related to differences in the exercise intensity, training status of participants, completion of
exercise in the fasted or postprandial state, timing of meal intake and analytical methods used to
quantifyhormoneconcentrations.
Sex-based differences in the regulation of appetite in response to acute exercise have been
examined directly in four studies [14,15,65,66]. The first acute exercise and appetite study that
compared men and women was published by Kawano and colleagues [65]. The authors reported
that20minofropeskippingexerciseincreasedratingsofsubjectivehunger30minafterexercisein
women but not men; however, the absence of a control condition in this study and the somewhat
unusual mode of exercise make this finding difficult to interpret. Furthermore, this study did
not control for the potential confounding effects of the menstrual cycle, which represents an
importantconsiderationforacuteexercisestudiescomparingmenandwomen. Inthisregard,recent
evidencesuggeststhatcomparedwithuntailoredprograms,synchronisingdietandexercisetraining
interventionsaroundthehormonalchangesthatoccurduringthemenstrualcycleelicitsgreaterweight
loss[67]andimprovementsinmusclestrength[68]. Inaddition,cyclicalfluctuationsinsexhormones
(estrogenandprogesterone)havebeenshowntoalterappetite-regulatoryhormoneconcentrationsand
energyintakeinwomenacrossthemenstrualcycle[69,70]. However,whetherappetiteresponsesto
exerciseinwomenareinfluencedbythemenstrualcyclephaseisnotknownandrepresentsaresearch
avenuetoconsiderinthefuture.
Subsequent studies directly comparing men and women have also incorporated measures of
appetite-regulatory hormones and energy intake (discussed below) alongside subjective appetite
perceptionstoprovideamorecomprehensivepictureofpotentialsex-baseddifferencesinappetite
regulation. In this regard, Hagobian and colleagues [14] examined the appetite and hormonal
.
responses to a single bout of cycling performed at 70% VO until 30% of total daily energy
2peak
expenditurewasexpendedinhealthymenandwomenmatchedforageandcardiorespiratoryfitness.
Importantly,thefemaleparticipantswereallstudiedduringtheearlyfollicularphaseofthemenstrual
cycle. Theauthorsreportedthatappetiteperceptionsandappetite-regulatoryhormoneconcentrations
(acylatedghrelinandPYY )werenotdifferentduringthe40minafterexerciseineithersex.Similarly,
3–36
Nutrients 2016, 8, 583  5 of 17
fitness. Importantly, the female participants were all studied during the early follicular phase of the 
menstrual cycle. The authors reported that appetite perceptions and appetite‐regulatory hormone 
Nutrients2016,8,583 5of18
concentrations (acylated ghrelin and PYY3–36) were not different during the 40 min after exercise in 
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70%peakoxygenuptake).†Significantdifferencebetweenexerciseandcontrolp≤0.05;*Significant
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differencebetweenwomenandmenp≤0.05.Valuesaremean(SEM),appetiteratings:n=10men,
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n=10women; acylated ghrelin: n = 8 men, n = 8 women. Data reproduced from reference [15].
©WoltersKluwerHealth,Inc.Reproducedwithpermission.
Nutrients2016,8,583 6of18
4.2. EnergyIntake
Manyofthestudieshighlightedaboveincludedanadlibitummealinthepost-exerciseperiod
toassesspotentialchangesinenergyintakeafterasingleexercisestimulus. Themajorityofstudies
in men report no change in absolute energy intake after acute exercise when a single or multiple
ad libitum meals are provided 30 min to 7.5 h after the cessation of exercise [48,49,52,53,55,71–73];
however,somestudieshavereportedincreases[50,74]ordecreases[47,58,75]inenergyintakeafter
acuteexercise. Nevertheless,twostudieshavedemonstratedthat24henergyintakeisunchanged
afteracuteexerciseinhealthymenquantifiedfromlaboratory-basedadlibitummealsandovernight
foodbags[48,52].
Similarly,evidencesuggeststhatadlibitumenergyintakeremainsunchangedinresponsetoacute
exerciseinhealthywomen[64,76–78]andoverweightandobesewomen[61,62,76]. Asanexception,
Larson-Meyerandcolleagues[64]reportedthatabsoluteenergyintake(adlibitummealprovided120
.
minafterexercise)wasunchangedafter60minrunningat70%VO ,butwasincreasedafter60
2peak
minwalkingperformedatthesamerelativeintensityinadifferentgroupofwomen. Thestrengthof
thisevidenceislimitedhoweverbythebetween-measuresdesignandthestarkdifferencesinbody
compositionandcardiorespiratoryfitnessbetweenthetwogroups. Inanotherstudy,Pomerleauand
colleagues[79]reportedthatadlibitumenergyintakewasincreased1hafterbriskwalkingat70%
.
VO inhealthy,youngwomen. However,thischangedidnottranslatetoalteredenergyintake
2peak
overtheremainderofthedayaftertheprovisionofanadlibitummeal6.5hafterexerciseandan
overnightsnackbag. Thishighlightstheimportanceofmonitoringfeedingbehaviouroverlonger
timeperiods.
Regardlessofwhetherabsoluteenergyintakeremainedunchanged,increasedordecreasedin
response to acute exercise in the studies cited thus far, relative energy intake (total energy intake
minusnetenergyexpenditureofexercise)isinvariablylowerafterexercisecomparedwithcontrol
inmenandwomen. Whilstthissuggeststhattheexercise-inducedenergydeficitismaintainedafter
exercise,whichmayhavesignificantimplicationsforweightmanagement,itshouldbenotedthatthe
short-termfollowupinthesestudiespreventsusfromdrawingconclusionsaboutbehaviouraland
physiologicalresponsesoveragreaterperiodoftime.
Studiesdirectlycomparingmenandwomenhavedemonstratedthattotalenergyintakeisgreater
inmencomparedwithwomen[14,15],butthisdifferencedisappearsafteradjustmentforleanbody
mass [15]. These findings coupled with the higher appetite ratings reported in men in the study
conducted by Alajmi and colleagues [15] lend support to the theory that lean body mass, as the
largestcontributortorestingmetabolicrate,isaprimarydeterminantofappetitecontrolandenergy
intake[24,25].
Inadditiontotheappetiteandhormoneresponsesdiscussedintheprevioussection,Hagobian
andcolleagues[14]reportedthatabsoluteenergyintakewasunchangedinresponsetoasinglebout
ofcyclinginducingasimilarenergyexpenditure(30%oftotaldailyenergyexpenditure)inmenand
women(energyexpenditure: men,975kcal;women,713kcal)(Figure2). Theauthorsobservedlarge
variabilityintheenergyintakeresponses(notelargeSDsonFigure2especiallyformen)withevidence
of both higher and lower energy intake after exercise compared with a resting control condition
in both men and women, which supports previous acute exercise and appetite regulation studies
in healthy weight [78] and overweight and obese [62] women. Although the authors reported no
significantchangeinenergyintakeafteracuteexerciseinmenorwomen,itisworthnotingthatmean
adlibitumenergyintakewashigherinmenafterexercise(Figure2)[14]. Acloserexaminationofthe
meandifferencesandestimatedstandardisedeffectsizesrevealedthatenergyintakeaftertheexercise
boutwas432kcalhigherthancontrolinmen(effectsize=0.68indicatingamoderatetolargeeffect)
comparedwitha1kcalincreaseafterexerciseinwomen(effectsize=0.004indicatingatrivialeffect)
(Figure2). Whilethisopposesthehypothesisthatwomenaremorelikelytocompensateforacute
exercise-inducedenergydeficitsbyincreasingenergyintake,theconclusionthatenergyintakewas
unchangedinmenshouldperhapsbeinterpretedwithcaution.
Nutrients 2016, 8, 583  7 of 17
compensate for acute exercise‐induced energy deficits by increasing energy intake, the conclusion 
tNhuattr ieenntser2g01y6 ,i8n,t5a8k3e was unchanged in men should perhaps be interpreted with caution.  7of18

Figure2. Totaladlibitumenergyintakeduringasinglelaboratory-basedbuffetmealinthecontrol
Figure 2. Total ad libitum energy intake during a single laboratory‐based buffet meal in the control 
((cid:3)) and exercise ((cid:4)) conditions in 11 men and 10 women. Exercise involved a single bout of
(□) and exercise (■) conditions in 11 men and 10 women. Exercise involved a single bout of cycling 
cycling performed at 70% peak oxygen uptake until 30% of total daily energy expenditure was
performed at 70% peak oxygen uptake until 30% of total daily energy expenditure was expended. * 
expended.*Significantdifferencebetweenwomenandmenp≤0.05.Valuesaremean(SD).Datafrom
Significant difference between women and men p ≤ 0.05. Values are mean (SD). Data from reference 
reference[14].©2008CanadianSciencePublishingoritslicensors.Reproducedwithpermission.
[14]. © 2008 Canadian Science Publishing or its licensors. Reproduced with permission. 
SSuubbsseeqquueenntt ssttuuddiieess iinnvveessttiiggaattiinngg ppootteennttiiaall sseexx‐-bbaasseedd ddiiffffeerreenncceess hhaavvee rreeppoorrtteedd nnoo cchhaannggee iinn 
aabbssoolluuttee eenneerrggyy iinnttaakkee iinn rreessppoonnssee ttoo aa ssiinnggllee bboouutt ooff rruunnnniinngg [[1155]] aanndd aaccccuummuullaattiinngg sshhoorrtt bboouuttss ooff 
wwaallkkiinngg ttoo bbrreeaakku upps esdeednetnatrayryti mtiem[e6 6[]6.6F].u rFtuhretrhmeromreo,rthe,e stheesstue dsiteusdhieasv ehcaovnes icsotennstislyternetplyo rrteedpoarltoewd ear 
lroewlaetirv reeelanteivrgey einnetragkye ainfttearkaec auftteere xaecructisee ecxoemrcpisaer ecdomwpitahrceodn wtroitlhi ncobnottrhols eixne sb,ostuhg sgeexsetsin, gsuthgagteastciuntge 
tehxaetr acicsuetesu epxperrceisssee dsurpeplarteivsseeedn reerlgaytivinet aekneerignyd einpteankdee inntdoefpseenxd[e1n4t, 1o5f, 6s6e]x. [14,15,66]. 
5. ChronicEffectsofExerciseonAppetite,Appetite-RegulatoryHormonesandEnergyIntake
5. Chronic Effects of Exercise on Appetite, Appetite‐Regulatory Hormones and Energy Intake 
Althoughacuteexercisestudiesprovideimportantinformationregardingappetiteregulation,
Although acute exercise studies provide important information regarding appetite regulation, 
exercisetrainingstudiesarerequiredtodiscernthelong-termeffectsofexerciseonenergybalance
exercise training studies are required to discern the long‐term effects of exercise on energy balance 
and weight control. Exercise training studies are now reviewed with continued focus on appetite
and weight control. Exercise training studies are now reviewed with continued focus on appetite 
sensations, appetite-regulatory hormones and energy intake responses between men and women.
sensations, appetite‐regulatory hormones and energy intake responses between men and women. It 
Itshouldbenotedthatfewwell-controlledexercisetrainingstudieshavebeenconductedwithmany
should be noted that few well‐controlled exercise training studies have been conducted with many 
studiesinherentlylimitedbymethodologicalconstraintssuchasunsupervisedexercise,self-reported
studies inherently limited by methodological constraints such as unsupervised exercise, self‐reported 
energyintake,lowexercise-inducedenergyexpenditureandalackofobjectivemeasurestoquantify
energy intake, low exercise‐induced energy expenditure and a lack of objective measures to quantify 
exerciseenergyexpenditure.
exercise energy expenditure. 
5.1. AppetiteandAppetite-RegulatoryHormones
5.1. Appetite and Appetite‐Regulatory Hormones 
Alterationsinghrelinconcentrationsafterchronicexercisehavebeenreportedinconjunctionwith
Alterations in ghrelin concentrations after chronic exercise have been reported in conjunction 
favourablechangesinbodyweight. Specifically,weightlossinresponsetoanexerciseintervention
with favourable changes in body weight. Specifically, weight loss in response to an exercise 
hasbeenshowntoelevatetotalghrelinconcentrationsinhealthyweightandoverweightandobese
intervention  has  been  shown  to  elevate  total  ghrelin  concentrations  in  healthy  weight  and 
womeninthefastedstateandpostprandially(reviewedby[40]). Incontrast,Guelfiandcolleagues[80]
overweight and obese women in the fasted state and postprandially (reviewed by [40]). In contrast, 
reportednoeffectof12weeksofaerobicorresistanceexerciseonfastingandpostprandialhungerand
Guelfi and colleagues [80] reported no effect of 12 weeks of aerobic or resistance exercise on fasting 
concentrationsofacylatedghrelinandPYYinoverweightandobesemen,despiteareductioninbody
and postprandial hunger and concentrations of acylated ghrelin and PYY in overweight and obese 
fatmassinbothexerciseinterventions. However,theauthorsreportedlowerfastingandpostprandial
men, despite a reduction in body fat mass in both exercise interventions. However, the authors 
leptinconcentrationsafterexercise,whichhasbeenobservedinotherstudieswithmenandwomen
reported  lower  fasting  and  postprandial  leptin  concentrations  after  exercise,  which  has  been 
afterexercise-inducedweightloss[81,82]. Furthermore,chronicexercisestudiesresultinginweight
observed  in  other  studies  with  men  and  women  after  exercise‐induced  weight  loss  [81,82]. 
lossinwomenappeartoreducefastinginsulinconcentrations[83,84],buthavelittleeffectonfasting
Furthermore, chronic exercise studies resulting in weight loss in women appear to reduce fasting 
totalPYYandGLP-1 concentrations[84,85].
7–36
Severalexerciseandappetitetrainingstudiesrecruitingbothmenandwomenhavepresented
findings with the data for men and women combined [36,86,87]. Although these studies are
Nutrients2016,8,583 8of18
informative, it is not possible to elucidate the direct effect of sex on the observed responses.
.
Nevertheless,short-termexercisetrainingwithoutweightloss(1hofdailywalkingat70%VO
2peak
for15days)resultedinnochangesinappetiteorcirculatingconcentrationsoftotalPYYandinsulinin
obesemenandwomen[87]. Martinsandcolleagues[36,86]haveperformedtwostudiesinvestigating
appetiteandappetite-regulatoryhormoneresponsestostandardisedmealsinoverweightandobese
men and women undertaking 12 weeks of supervised aerobic exercise resulting in weight loss.
Theexerciseinterventionreducedfastinginsulinconcentrationsbutresultedinanincreaseinfasting
acylatedghrelinconcentrationsandhungerperceptions[36]. Inthepostprandialstate,circulating
insulinwasreducedalongwithagreatersuppressioninacylatedghrelinandatendencyforincreased
PYY and GLP-1 concentrations compared with levels before the intervention [36]. Furthermore,
fastingandpostprandialconcentrationsofleptinwerereducedaftertheexerciseintervention[86].
Thesefindingsledtheauthorstoconcludethatinresponsetochronicexercise,overweightindividuals
maybalancetheincreaseddrivetoeatwithaconcomitantincreaseinthesatietyresponsetoameal,
whichsupportspreviousfindingsinoverweightandobesemen[38].
In many of the studies discussed thus far, participants maintained their usual diet and
subsequentlylostbodymassandfatmassbytheendofthechronicexerciseintervention.Therefore,itis
difficulttodeterminewhetherthereportedexercise-inducedchangesinappetitecontrolareattributable
toweightlossortoexercisetrainingperse. Inthisregard,thestudybyKanaleyandcolleagues[87]
discussedpreviouslydidnotreportchangesinappetiteorappetite-regulatoryhormones(totalPYY,
and insulin) in response to short-term exercise training without weight loss. Furthermore, total
ghrelin concentrations were unchanged after exercise training in women who did not experience
weightloss[85,88],andastudyconductedinoverweightadolescentsobservednochangesinfasting
acylated ghrelin when body weight remained stable during the eight-month supervised exercise
intervention [89]. Therefore, it is likely that alterations in appetite-regulatory hormones arise as a
secondaryconsequencetochangesinbodymass.
Earlyevidenceofexercise-inducedsexdifferencesinappetitehormoneswasprovidedbyHickey
andcolleagues[90]. Inthisstudy, 12weeksofaerobicexercisetraining, withoutachangeinbody
massorbodyfat,significantlyreducedfastinginsulinandleptinconcentrationsinwomenbutnot
inmen. Subsequently,Hagobianandcolleagues[13]examinedappetitehormoneresponsestomeal
intakebeforeandafterfourconsecutivedaysofexerciseinpreviouslysedentaryoverweightandobese
.
menandwomen. Dailyaerobicexercisewasperformedonatreadmillat50%–65%VO resulting
2peak
inanenergyexpenditureequivalentto~30%oftotaldailyenergyexpenditureandwascompleted
withandwithoutdietaryreplacementoftheexercise-inducedenergydeficit. Theauthorsreported
thatacylatedghrelinconcentrationswerehigherandinsulinconcentrationswerelowerafterboth
exerciseinterventionsinwomen(Figure3). Incontrast,althoughmendemonstratedlowerinsulin
concentrationsintheenergydeficitcondition,thiseffectwaseliminatedwithenergyreplacementand
acylatedghrelinwasnotdifferentafterexerciseregardlessofenergystatus(Figure3). Thesefindings
suggestthatwomenexperienceperturbationsinappetite-regulatoryhormonesconducivetoappetite
stimulationinresponsetotheinitiationofexercisetraining. Thisisconsistentwiththehypothesisthat
themechanismsgoverningenergybalancearemoretightlyregulatedinwomenthanmen.
However, in the Midwest Exercise Trial, lower insulin concentrations were observed in men
butnotwomenafterthe16-monthexercisetrainingintervention[32]. Thiswasaccompaniedbya
divergentweightlossresponsetoexercisetraining(discussedpreviously)which,coupledwiththe
greaterexerciseenergyexpenditureinmen,islikelytoexplainthedifferentialinsulinfindingsbetween
thisinvestigationandthatofHagobianandcolleagues[13].
Althoughreplacingtheexercise-inducedenergydeficitsuppressedappetiteperceptionsinmen
butnotwomen,appetitewasnotalteredwhentheenergydeficitwasmaintainedineithersex[13].
Thissupportsapreviousstudyreportingnochangeinpostprandialappetiteinresponseto14days
of moderate- or high-intensity exercise training in lean men and women [91]. In another study,
sex-baseddifferencesinbodyweightandappetitewereexaminedinresponsetoa12-weeksupervised
Nutrients2016,8,583 9of18
aerobic exercise intervention in overweight and obese men and women [8]. The 12-week exercise
programresultedinsimilarreductionsinbodymassandbodyfatinthemaleandfemaleparticipants.
Furthermore,althoughfastinghungerratingswereelevatedaftertheexercisetrainingintervention,
themagnitudeofchangewassimilarbetweenthesexesandthisdifferencedidnottranslatetoaltered

Nutrients 2016, 8, 583  9 of 17
hungerresponsesinthepostprandialperiod.

Figure 3. Total area under the curve (AUC) for plasma acylated ghrelin (a) and insulin (b)
cFoignuceren tr3a. tiToontsailn atrheea counntdreorl (t(cid:3)h)e, ecxuerrvceis e(AwUitCh)e nfoerr gpyladsemficai ta(c(cid:4)y)laatnedd egxherrecliisne w(ai)t haennde rignysublainla n(cbe) 
(c(cid:4)on)cceonntdraittiioonnss iinn tnhien ecomnternola (n□d), neixneercwisoe mweitnh. eEnxeerrgcyis deeifnivciot l(v■e)d anfodu erxceorncisseec wutiitvhe ednaeyrgsyo bfatrlaenadcem (■ill) 
conditions in nine men and nine women. Exercise involved four consecutive days of treadmill 
exerciseat50%–65%peakoxygenuptakeuntil30%oftotaldailyenergyexpenditurewasexpended.
*exSeigrcniisfiec aatn 5t0d%if–f6e5re%n cpeeabke towxeyegnene xueprtcaiskee iunntetirlv 3e0n%ti oonf taontadl cdoaniltyro eln;e†rSgiyg nexifipceanndtitduirfefe wreansc eexbpeetnwdeeedn.  
* Significant difference between exercise intervention and control; † Significant difference between 
exercisewithenergydeficitandexercisewithenergybalance.Valuesaremean(errorbarsnotstated
exercise with energy deficit and exercise with energy balance. Values are mean (error bars not stated 
in original article). Data reproduced from reference [13]. © The American Physiological Society.
in original article). Data reproduced from reference [13]. © The American Physiological Society. 
Reproducedwithpermission.
Reproduced with permission. 
5.2. EnergyIntake
Although replacing the exercise‐induced energy deficit suppressed appetite perceptions in men 
but nCout rwreonmteevni,d aepnpceetsitueg wgeasst sntohta atlitnecrreeda swinhgenen tehreg yeneexrpgeyn ddietfuicriet dwuarsin mgasihnotrati-nteerdm ine xeeitrhciesre steraxi n[1in3]g. 
(T3htios 1su4pdpaoyrst)se ali cpirtsevpiaorutisa sltcuodmyp reenpsoarttiionngs nino ecnhearnggye iinnt apkoest[p91ra–n94d]i.aFl uarptpheetrimteo irne ,reasrpeocennset styos 1te4m daatyics 
roefv miewodceornatcelu‐ doerd htihgaht‐lionntegnesritteyr mexeexrceirscei steratrianiinnign gins tuledaine sm(>e2nw aenedk swtoom18enm o[9n1th].s )Inty apnicoatlhlyero bstsuerdvye, 
nseoxc‐bhaasnegde idnieffneerregnyceins taink ebaocdroys swtheeigthrat inainndg ianpteprevteitnet iowne[r9e5 ]e.xHaomwineevder ,itnh ereasupthoonrsse retcoo gan i1s2e‐dwteheakt 
tshuepaevrvaiilsaebdl eaelirtoerbaitcu erxeeirscpisreo ninetteorvveanritoiouns mine othvoedrwoleoiggihcta lasnhdo ortbceosme imngesna asnhdig whloigmhetned [8p]r. eTvhioeu 1s2ly‐w(ee.egk., 
uexnesrucpiseer vpirsoegdreaxme rrceissue,ltseedlf -irne psiomrtieladr erneedrugcytiionntas kine) bwohdiyc hmmasask aesndit bdoifdfiyc ufaltt tioni nthteer mpraeltet hanedfi nfedminagles 
wpaitrhticciopnafindtse.n Fcue.rthermore, although fasting hunger ratings were elevated after the exercise training 
intervAenreticoenn,t tshteu dmyadgnirietcutdlye coof mchpaanrigneg wisaose nsiemrgileatri cbtehtwreeee-dna tyhee nseerxgeys danefidc tithsisi mdpifofesreedncbey ddidie tnoort 
etrxaenrscliasteer teop aolrtteerdedt hhautndgieert arreysproenstsreics tiino nthset ipmoustlpatreadndaiaclo pmeprieonds.a toryincreaseinadlibitumenergy
5.2. Energy Intake 
Current  evidence  suggests  that  increasing  energy expenditure during  short‐term  exercise 
training (3 to 14 days) elicits partial compensations in energy intake [91–94]. Furthermore, a recent 
systematic review concluded that longer term exercise training studies (>2 weeks to 18 months) 
typically observe no change in energy intake across the training intervention [95]. However, the
Nutrients2016,8,583 10of18
intakethatwasnotobservedinresponsetoexercise[96]. Thissupportsthefindingsfromacutestudies
demonstratingrapidcompensatorychanges(appetite,appetite-regulatoryhormones,energyintake)in
responsetodiet-,butnotexercise-inducedenergydeficitsinmen[71]andwomen[15]. Thesefindings
suggestthatdietaryrestrictionmayrepresentagreaterchallengetoappetiteregulationandenergy
balancethanexercise,highlightingtheimportanceofexercisetofacilitateweightmanagementinmen
andwomen[3].
Apotentialsexdifferenceinenergyintakeresponsesduringshort-termexercisetrainingwas
uncoveredintwoseparatestudiesbyStubbsandcolleagues[93,97]. Specifically,theauthorsreported
that increasing energy expenditure through exercise training (seven days daily moderate- or
high-intensityexercise)resultedinapartialcompensationinenergyintakeinhealthywomenthat
equatedto~33%oftheadditionalexercise-inducedenergyexpenditure[93]. Incontrast,therewas
nocompensationintheenergyintakeresponsetoanidenticaltrainingstimulusinhealthymen[97].
However,itisworthnotingthatenergyintakewasself-recordedinthesestudiesthroughsubjective
dietary records and self-weighed intakes. This method of recording energy intake is particularly
susceptibletoparticipantbias,whichmakesitchallengingtoreconcileself-reportedfoodintakewith
actualintake[98].
Inasubsequentstudyadoptingobjectivemeasuresofbothenergyintakeandenergyexpenditure,
evidenceofpartialcompensationsinenergyintakeemergedafter14daysofsuperviseddailyexercise
whichwasequivalentto~30%oftheexercise-inducedenergydeficit[91]. Thisresponsewasobserved
whenenergyintakedatawerecombinedformenandwomen,butonlyreachedsignificanceinmen
whenanalysedindependentlybysex[91]. Thisisconsistentwithanearlystudydemonstratingthat
men,butnotwomen,increaseenergyintakeinresponsetofivedaysofdailyexercise,yetneithersex
fullycompensatedfortheimposedexerciseenergyexpenditure[92]. Consequently,thesefindings
refutethehypothesisthatwomencompensateforchronicexercise-inducedenergydeficitsbyincreasing
energyintake.
When data is combined for men and women, studies investigating the effect of 12 weeks
of supervised exercise (five days·week−1, 500 kcal·session−1) on body composition and appetite
controlhavereportednoexercise-inducedchangeinenergyintakeassessedusingself-reportedfood
diaries[36]orlaboratory-basedtestmeals[99]. Furthermore,Westerterpandcolleagues[5]reported
no significant change in energy intake assessed using a self-reported seven-day weighed diary in
menorwomenafter40weeksofendurancetraining. IntheMidwestExerciseTrials,energyintake
wasassessedusingacombinationofadlibitummealsintheUniversitycafeteriaand24hrecallin
overweightandobesemenandwomenundergoingasupervisedaerobicexerciseprogramfor10[9]
or16months[6]. Similarly, nodifferenceinenergyintakewasreportedaftertheexercisetraining
interventionsineithersex[6,9].
Whenexerciseissupervisedandenergyintakeisquantifiedobjectivelyusinglaboratory-based
adlibitummeals,nochangesindailyenergyintakewereobservedinoverweightandobesemenor
women after a 12-week aerobic exercise intervention (Figure 4) [8]. The authors of this study also
highlightedthelargevariabilityinindividualweightlossresponses,bothinmagnitudeanddirection,
whichmayaffordsomeinsightintowhymanyindividualsdonotachievetheirpredictedchangesin
bodycompositionwithchronicexercise.Suchheterogeneityinresponsetoalterationsinenergybalance
hasbeenrecognisedpreviously[8,9,29,35,37,38]. Interestinglyandpertinenttothisreview,overweight
andobesemenandwomentypicallydemonstrateasimilardegreeofindividualvariabilitywhenthe
exercise-inducedenergyexpenditureisequivalentbetweenthesexes[8,38]. Forexample,Caudwell
andcolleagues[8]reportedbodymasschangesrangingfrom −14.7to2.0kginmenand−10.0to
4 kg in women. Furthermore, when participants are retrospectively classified as “responders” or
“non-responders”(basedontheiractualweightlossrelativetotheirpredictedweightloss),thereis
someevidencesupportinghigheradlibitumenergyintakeinindividualsexperiencinglowerthan
theirpredictedweightloss[29,37,38].