Clinical Study Influence of Running and Walking on Hormonal Regulators of Appetite in Women

16 Pages·2014·1.42 MB·English

HindawiPublishingCorporation
JournalofObesity
Volume2012,ArticleID730409,15pages
doi:10.1155/2012/730409
Clinical Study
Influence of Running and Walking on Hormonal Regulators of
Appetite in Women
D.EnetteLarson-Meyer,1SonniePalm,1AasthaaBansal,2KathleenJ.Austin,3
AnnMarieHart,4andBrendaM.Alexander3
1DepartmentofFamilyandConsumerSciences,UniversityofWyoming,Laramie,WY82071,USA
2DepartmentofBiostatistics,UniversityofWashington,Seattle,WA98195,USA
3DepartmentofAnimalScience,UniversityofWyoming,Laramie,WY82071,USA
4FayW.WhitneySchoolofNursing,UniversityofWyoming,Laramie,WY82071,USA
CorrespondenceshouldbeaddressedtoD.EnetteLarson-Meyer,[email protected]
Received14October2011;Accepted22December2011
AcademicEditor:PietroForestieri
Copyright©2012D.EnetteLarson-Meyeretal. This is an open access article distributed under the Creative Commons
AttributionLicense,whichpermitsunrestricteduse,distribution,andreproductioninanymedium,providedtheoriginalworkis
properlycited.
Nine female runners and ten walkers completed a 60min moderate-intensity (70% VO max) run or walk, or 60min rest in
2
counterbalanced order. Plasma concentrations of the orexogenic peptide ghrelin, anorexogenic peptides peptide YY (PYY),
glucagon-likepeptide-1(GLP-1),andappetiteratingsweremeasuredat30minintervalfor120min,followedbyafree-choice
meal.Bothorexogenicandanorexogenicpeptideswereelevatedafterrunning,butnochangeswereobservedafterwalking.Relative
energyintake(adjustedforcostofexercise/rest)wasnegativeinthemealfollowingrunning(−194±206kcal)versuswalking
(41±196kcal)(P=0.015),althoughbothweresuppressed(P<0.05)comparedtorest(299±308and284±121kcal,resp.).The
averagerateofchangeinPYYandGLP-1overtimepredictedappetiteinrunners,butonlythechangeinGLP-1predictedhunger
(P=0.05)inwalkers.Resultsprovideevidencethatexercise-inducedalterationsinappetitearelikelydrivenbycomplexchanges
inappetite-regulatinghormonesratherthanchangeinasinglegutpeptide.
1.Introduction Although the aforementioned recommendations, if fol-
lowed, are likely to have a major impact on health, inter-
Thebenefitsofexerciseinthepreventionofchronicdiseases vention studies find that exercise without intentional food
includingoverweightandobesityarewelldocumented.Reg- restrictionand/orbehaviormodificationdoesnoteffectively
ularphysicalactivityreducesbloodpressure,createsamore promote weight loss, [5, 6], particularly in women [7, 8].
favorablelipidprofile,andreducesriskforstroke,coronary Thismaybebecauseexercisestimulatesacompensatory(rel-
heartdisease,hypertension,andcoloncancer[1,2].Regular ative to the energy expenditure of the activity) or noncom-
exercisealsohelpsmaintainhealthybodyweight[1]andmay pensatorydrivetoeatthatiseitherbiologically—(i.e.,alter-
aidinweightlossandweightlossmaintenance[3].Tohelp ed appetite regulating hormones) or psychologically—(i.e.,
prevent weight gain (or obesity), the 2008 Physical Activity feeling one deserves dessert after exercising) driven. These
Guidelines for Americans [4], sponsored by the Centers studies, however, are not consistent with short-term exper-
for Disease Control and Prevention and Healthy People imentalstudiesconductedmostlyinmenwhichhavefound
2020,suggestsincorporatingaminimumweeklytotaloftwo reductions in appetite and relative food intake following
andahalfhoursofmoderate-to-vigorousintensityphysical moderately intense-to-vigorous exercise. This may be be-
activity, spread over most days of the week. Working up to causetheexercise-inducedeffectisinfluencedbyfactorsin-
fiveormorehoursperweek(∼60min/day)isrecommended cluding the intensity and mode of the exercise [9–11], the
to gain additional benefits which include weight loss and sex, and body composition of the exerciser [9, 10]. Several
weightlossmaintenance. previous studies found that hunger and/or food intake are
2 JournalofObesity
suppressed following 30–90min of intense- but not neces- gastrointestinal, pulmonary, cardiac, or hematological dis-
sarilylight-to-moderateintensityexercise[12–18]including eases including high blood pressure (>120/80mm/Hg at
cycling, running, and brisk walking. Others reported in- rest),prediabetes/diabetes,demonstratedsignsofsignificant
creasesinhungerandfoodintakefollowingswimming[19] depression, anxiety, other psychological problems, alcohol-
and exercise calisthenics [20]. Less is known concerning ismorothersubstanceabuse,usedprescriptionoroverthe
individualdifferences;however,onestudyfoundsuppressed counter medications (other than contraceptives), or herbal
hunger and food intake in lean but not overweight women preparationsthatcaninfluencemetabolism,hadfoodaller-
followingbicycleexercise[21]. gies,orwereunwillingtoconsumeallfoods/beveragespro-
The recent discovery of several gut peptides involved in videdintherun-indiet.ThestudywasapprovedbytheIn-
appetite regulation and energy homeostasis provides an at- stitutionalReviewBoardoftheUniversityofWyoming.Vol-
tractive mechanism to explain how exercise reduces hung- unteerswerefullyinformedofpossiblerisksofallprocedures
er/appetiteinsomeconditionsandincreasesitinothers.Al- beforeprovidingwritteninformedconsent.
terations in circulating ghrelin, the only known orexigenic
gutpeptide,alongwiththeanorexigenicgutpeptidespeptide
2.1.BaselineTesting. Approximatelytwoweeksbeforeiniti-
YY(PYY)andglucagon-likepeptide-1(GLP-1)mayworkin
ationoftheexperimentalprotocol,VO maxwasdetermined
concerttoinfluenceexercise-associatedalterationsinhunger 2
onamotor-driventreadmill(TrackmasterTMX22,Newton,
and food intake. Alterations in circulating gut peptides ap-
KS,USA)inaccordancewithACSMrecommendations[29].
pear to regulate food intake for as long as 24h and are not
Formostrunners,testingwasinitiatedat6mph(0%grade)
specificallycontrolledbybodyfatstores.Anumberofprevi-
withthegradeincreasingby1%everyminuntilexhaustion.
ousstudieshavefoundthatthesepeptidesarealteredbyan
Forthewalkers,thetestwasinitiatedat3.5mph(2%grade)
acuteboutofexercise[16,17,22–28];however,themajority
with grade increasing by 1% every min until exhaustion.
ofstudiesevaluatedonlyasinglemodeofexercisecompared
Oxygenconsumption(VO )andcarbondioxideproduction
torest.Inaddition,onlyafewofthesestudiessimultaneously 2
(VCO )weremeasuredcontinuouslyusingametaboliccart
evaluatedboththeorexogenicandanorexogenicgutpeptides 2
(ParvoMedics TureOne 2400, Sandy, UT, USA), and heart
[17,27,28],andfewincludedwomen[23,27,28].
rate(HR)wasmonitoredbyanelectrocardiographymachine
The purpose of this study was to assess the effect of a
(Quinton Q-5000, Bothell, WA, USA). Rating of perceived
60-minuteboutofexerciseoncirculatingconcentrationsof
exertion (RPE) was assessed during the last 10 seconds of
gut peptides ghrelin, PYY, and GLP-1; appetite and ad libi-
each stage using the modified Borg Scale [29]. The highest
tumfoodintakeamongwomen.Anadditionalpurposewas
20-secondVO andrespiratoryexchangeratio(RER)achie-
to assess whether alterations in these gut peptides were as- 2
vedinthefinaltwominofexercisewererecordedasthemax-
sociatedwithalterationsinappetitefollowingexercise.Exer-
imumvalues.Toqualifyasanacceptablemaximumtest,par-
cisewasperformedatamoderatelyhardintensityintwodif-
ticipants had to meet two of the four following criteria:
ferent modes: running and walking. We hypothesized that
(1) a leveling or plateau of VO (defined as an increase of
circulating ghrelin would be suppressed; PYY and GLP-1 2
<2mL·kg−1·min−1 with increased workload); (2) RER ≥
concentrations elevated following both modes of exercise
1.10; (3) maximum heart rate within 10 beats of age pre-
comparedtorest.Furthermore,wehypothesizedthatghrelin
dictedmaximum[208−(0.7×age)][30];(4)ratingofper-
concentration would be directly correlated with ratings of
ceivedexertion(RPE)≥17.Aftera30minrecoveryperiod,
hungeranddesiretoeatandPYYandGLP-1concentrations
participantsunderwentatitrationrun/walktodeterminethe
wouldbeindirectlycorrelated.
speedandgraderequiredtoelicitanoxygenuptakeof70%
VO max. For descriptive purposes, body composition was
2
measured using dual-energy X-ray absorptiometry (DEXA,
2.Methods
GELunarProdigy8743,Waukesha,WI,USA).
Nine endurance-trained female runners and ten habitual
walkers between the ages of 18–40 were recruited for the 2.2.ExperimentalProtocol. Thestudywasacounterbalanced,
study. To qualify, participants had to be in good general cross-over study where participants completed an exercise
health,havenormalhemoglobin(between14.0–18.0mg/dL) andcontrol(rest)testday.Aschematicofthestudyisshown
and thyroid status (thyroid stimulating hormone between in Figure1. The two test trials were scheduled in the fol-
0.40–4.50mlU/L),haveregularlyoccurringmenstrualcycles, licular phase of the participants’ menstrual cycle (between
andbeof“lowexerciserisk”aspertheAmericanCollegeof days1and11)andspacedeither2to10daysor1menstrual
Sports Medicine (ACSM) [29]. The runners had to be cur- cycle (3 to 5 wks) apart. The exercise test day consisted of
rently running at least 32km/wk, be performing runs of at a 60min run/walk at 70% VO max followed by 2h of rest,
2
least 60min in duration as part of their training regiment, whereasthecontroldayconsistedof3hofrest.Foodintake
and have maximal aerobic capacity (VO max) of at least wascontrolledfor24hpriortoeachtestdaybyprovidingpa-
2
45mL/kg/min. The walkers had to be performing walks of rticipantswithacontrolleddiet.Thedietprovided2000kcal
atleast60minindurationthreeormoredays/wkandhave (64% carbohydrate, 14% protein, and 22% fat) from com-
aVO maxoflessthan40mL/kg/min.Participantswereexc- merciallyavailablefoodsandbeveragesplusanoptionalad-
2
luded if they smoked, wereanemic, hyper-or hypo-thyroid, ditional200kcalprovidedastwo100kcalsnackbars(28.4g,
pregnantorpostmenopausal,hadrenal,hepatic,endocrine, ∼100kcals; Clif Bar and Company, Berkeley, CA, USA).
JournalofObesity 3
19 females
Runnersn=9
Walkersn=10
Exercise day Control day
•Follicular phase of menstrual cycle (cid:129)Follicular phase of menstrual cycle
(cid:129)Standard breakfast 120 min before (cid:129)Standard breakfast 120 min before
(cid:129)Pre-exercise blood draw (cid:129)Prerest blood draw
(cid:129)60-min run/walk @ 70% VO2max (cid:129)60 min rest (30 min resting metabolic
(cid:129)Blood draws every 30 min for 2 h rate via indirect calorimetry)
(cid:129)Hunger ratings prior to blood draws (cid:129)Blood draws every 30 min for 2 h
(cid:129)Hunger ratings prior to blood draws
(cid:129)Ad libitum meal 2 h after exercise
(cid:129)Ad libitum meal 2 h after rest
Figure1:Schematicofthecounter-balancedcross-overstudy.
Volunteerswereaskedtoconsumethefoodsprovided(and with a word describing the extremes of the appetite being
nothing in addition other than water) and to return empty measured[32].Thescalesspecificallyasked(1)howhungry
wrappers and any food and beverages that could not be doyoufeel?(2)howsatisfieddoyoufeel?;(3)howfulldoyou
consumed. feel? (4) how much do you think you can eat? Hunger and
satiety ratings were obtained 4 to 5min before each blood
draw(t=0,30,60,90,and120)andat20minafterinitiation
2.3. Test Days. On both test days, participants consumed a
oftheadlibitummeal(seebelow).
standard breakfast (Boost Smoothie, Clif Builder Bar and 2
Atcompletionoftheexerciseandrestsessions(120min),
cups of water; ∼380kcal; 65% carbohydrate, 20% protein, participantswereofferedanadlibitum,free-choicemeal.The
15%fat)at0630priortoarrivinginthelaboratory.At0730,
free-choicemealconsistedofthefollowing(inweighedpor-
height, weight, and blood pressure were measured. On the
tions) attractively and consistently arranged on the dining
control visit, an intravenous indwelling (IV) catheter was
table: rigatoni pasta (140g dry, cooked), marinara sauce
insertedintoanarmorhandveinandconnectedtoanormal
(140g), alfredo sauce (140g), whole-wheat bread (2 slices),
salinesolution(0.9%salinesolution)thatwasslowlyinfused
white bread (2 slices), hard boiled eggs (2), apples (2), or-
to keep the catheter patent. Blood was drawn immediately
anges (2), Clif snack bar (2), Clif Builder bar (2), nonfat
before(baseline,preexercise)andimmediatelyafteronehof
yogurt(1,6oz),regularyogurt(1,6oz),individualportions
rest (t = 0min) and every 30min thereafter for 2h (t =
ofmargarine(4),honey(4),peanutbutter(4),assortedjel-
30, 60, 90, 120min). The first 3cc at each time point draw
lies (4), lemon-lime Gatorade (2, 20oz), 2% milk (2, 8oz),
was presumed to be diluted with saline and was discarded.
and water (∼1500g). Participants were given 20min to eat
Resting energy expenditure (REE) and respiratory quotient
themealandwereinstructedtoeatuntilsatiety.Participants
(RQ)weremeasuredusingametaboliccart(160lpmpneu-
were not allowed to read or study during the meal or carry
matach,ParvoMedics,TrueOne2400,Sandy,UT,USA)while
backpacks, purses, or coats into the room. They were dis-
the subject lay motionless in the supine position, as previ-
cretelymonitoredbythesameinvestigatorwhoworkedqui-
ouslydescribed[31].Thelast20minofdatawasusedtocal-
etlyonacomputerinthebackoftheroom(withtheirback
culateREE.
turned toward the participant). Food and water consump-
On the exercise day, baseline blood was obtained by
tion were determined by weighing remaining food (to the
venipuncture.AnIVcatheterwasinsertedimmediatelyfol- nearest 0.1g) at cessation of eating. By difference, food/be-
lowing the 60min run/walk, and blood was drawn on the
veragesconsumedwereanalyzedfortotalenergy,protein,fat,
same schedule as the rest day. For 10min at the beginning
carbohydrate,simplesugars,andfiberusingNutritionistPro
(between5–15minafterthestart)andend(last5min)ofthe (Axxya Systems, Stafford, TX, USA, 77477). Ad libitum wa-
run/walksession,VO ,VCO ,RERandRPE,weremeasured
2 2 terintakeandintakeofenergyandmacronutrientsassolids
usingametaboliccart(800lpmpneumatach,ParvoMedics,
andliquidswerealsoassessed.Relativefoodintakewascal-
TrueOne2400,Sandy,UT,USA).Exercisepacewasadjusted,
culatedbysubtractingestimatedenergyexpenditureduring
ifnecessary,duringthefirst10mintoachieveanoxygencost
theexercise(60minexercise,120minrest)orrest(180min
ascloseto70%VO maxaspossiblebutwasnotfurtherad-
2 rest)sessionsfromtherespectivefree-choiceenergyintake.
justed. HR was monitored continuously using a portable
heartratemonitor(PolarS60i,Polar,PortWashington,NY,
USA). 2.4. Blood Samples and Hormone Analysis. Blood samples
Onbothtestdays,hungerandsatietywereassessedusing takenbothbeforeexerciseandrest(baseline)wereanalyzed
100mmvisualanaloguescales(VASs),anchoredateachend for serum concentrations of progesterone concentration
4 JournalofObesity
usingahumansolidphaseRIAkit(SiemensDiagnostics,Los calculated robust standard errors that accounted for corre-
Angeles, CA, USA). Plasma samples were analyzed for total lation between exercise and rest measures from the same
ghrelin, acylated ghrelin (ghrelin ), PYY , GLP-1, glu- subject. As a way of capturing total response over all time
acyl 3-36
cose, lactate and hematocrit at pre-exercise/rest and for points, the area under the curve (AUC) was also calcula-
120min following exercise and rest were analyzed for total ted for the 120 minutes following exercise and rest for the
ghrelin, acylated ghrelin (ghrelin ), PYY , GLP-1, glu- gut peptide concentrations and hunger ratings using the
acyl 3-36
cose,lactate,andhematocrit.Bloodsamplesfortotalghrelin, trapezoid method (GraphPad Prism version 5.02 for Win-
ghrelin , PYY , and GLP-1 were collected into EDTA- dows,GraphPadSoftware,SanDiego,CA,USA,http://www
acyl 3-36
treatedprechilledtubes.Bloodcollectedforanalysisofplas- .graphpad.com/).AUCincluded,bydefinition,theareaun-
ma ghrelin was collected into a chilled tube containing der the curve and above baseline. For ghrelin, ghrelin ,
acyl acyl
100µLof200mMAEBSFwith200µLof1NHCladdedper andGLP-1whichwereobservedtodipbelowbaselineinthe
mLofplasmafollowingcentrifugation.Samplescollectedfor later postexercise period, negative AUC was also calculated
analysis of PYY were treated with 150µL of aprotinin and astheareaabovethecurveandbelowbaseline.Pairedt-tests
40µLDPP-IV.Allplasmasampleswerecold-centrifuged(2– were used to evaluate differences between exercise and rest
8◦C) for 10min at 3500rpm. Aliquots of supernatant were responsesovertheentireperiodof120minutesafterexercise
storedincryovialsat−80◦Candbatch-analyzedinduplicate orrest,withinrunnersandwithinwalkers.Adlibitumfood
atstudycompletionbyradioimmunoassayusingcommerc- intakewasmeasuredatasingletimepointfollowingthead
iallyavailablekitsspecificforhumans(Millipore,St.Charles, libitum meal, as absolute energy intake and relative energy
MO,USA).Bloodsamplesforanalysisofglucoseandlactate intake. Again, paired t-tests were used to compare exercise
werecollectedinto4mLpurpletopvacutainers,centrifuged versusrestwithinrunnersandwithinwalkers.Assecondary
asabove,andtheplasmawasstoredat−80◦Cuntilanalysis. outcomes, we also considered more specific components of
Glucose and lactate were analyzed using a Microstat Multi- energyintake,usingthreemacronutrients:protein,carbohy-
assayAnalyzer(Analoxinstruments,Lunenburg,MA,USA). drate,andfat.Asanexploratoryanalysisrelatingtothisaim,
Hematocritwasanalyzedasamarkerofhemoconcentration wealsoassessedtheimmediateeffectsofexerciseversusrest
and hemodilution using an Autocrit Ultra 3 (Clay Adams, on gut peptide concentrations and appetite. That is, rather
Sparks,MI,USA)ateachblooddraw. than considering the trajectory of each outcome across all
time points from t = 0 to t = 120, we considered only the
difference between the measurements att = 0 and at base-
2.5. Statistical Approach. A sample size analysis conducted lineforexerciseversusrest.Withthesedifferencesastheout-
with mean and standard deviation estimates based on pre- comes,wefitlinearregressionmodels,includinganinterac-
liminary exercise-associated data from Russel et al. [28] in tion between exercise/rest and runner/walker group. Again,
women (n = 10) and Martins et al. [33] in both sexes wecalculatedrobuststandarderrorsthataccountedforcor-
(n=6men,6women)forthepre-topost-exercisechangein relation between exercise and rest measures from the same
PYY (15to25%increasewithexercise;SDsproportional subject.
3-36
to means; ratio of SD to mean = 0.26) and an alpha = 0.05 Our second aim was to investigate whether changes in
determinedthatasamplesizeofn = 8wassufficienttode- ghrelin, ghrelin , PYY, and GLP-1 were associated with
acyl
tect, with 80% power, a minimal postexercise increase of changes in hunger following exercise. For each gut peptide,
∼20% (http://www.statsalive.com/). Given this calculation, wefitalinearregressionmodelwiththepeptideconcentra-
ann=9foreachexercisegroup(i.e.,oneadditionalsubject tionasthepredictorofinterestandhungerastheoutcome.
pergroup)wasselected.Thesamplesizecalculationwasnot Additionally, we included an interaction between hormone
performedusingghrelinorghrelin duetoinconsistentre- levelandrunner/walkergroupandadjustedforbaselinehun-
acyl
sultsforghrelinandlackofpublishedresultsforghrelin . gerratingandexercise/restperiod.Again,wecalculatedrob-
acyl
Our first aim was to assess the effect of exercise on cir- ust standard errors to account for multiple measures from
culatingconcentrationsofgutpeptides,appetite,andadlibi- thesamesubject.Theotherappetiteratingswerealsoasses-
tum food intake among runners and among walkers. Con- sedassecondaryoutcomes.Statisticalanalyseswereperfor-
centrations of the gut peptides (total ghrelin, ghrelin ; medusingStata(version10)andRstatisticalsoftware(ver-
acyl
PYY and GLP-1), and the primary measure of appetite, sion 2.10.1). All reported P values were two-sided, with
3-36
hunger ratings were measured at baseline and five time statisticalsignificancetakentobeP value<0.05.Therewas
points(t = 0,30,60,90,and120minutes)followingexer- noadjustmentformultipletesting.
ciseandrest.Assecondaryoutcomesrelatingtoappetite,we
alsoconsideredratingsofsatiety,fullness,anddesiretoeat.
For each subject, we summarized the repeated measures by 3.Results
calculating the slope or the rate of change in outcome per
30-minute interval, following exercise and rest. Using the Nineteen volunteers (9runnersand 10 walkers)enrolledin
derivedslopesastheoutcome,linearregressionmodelswere the study. The majority of the runners regularly competed
fittoevaluatedifferencesbetweenexerciseandrestresponses inlocalroadracesandtwowereNCAAdivisionIcollegiate
over the entire period of 120 minutes following exercise or runners.Thewalkerswalkedregularlyeitherforfitnessand
rest. We adjusted for baseline levels and included an inter- weightcontrol,orascross-trainingforotheractivities.None
action between exercise/rest and runner/walker group. We of the walkers, however, were regular runners or joggers.
JournalofObesity 5
Table 1: Baseline preexercise characteristics for 9 female runners and 10 female walkers. Data are presented as mean ± SD. Body fat
percentagebydual-energyX-rayabsorptiometry;VO max:maximaloxygenuptakewhilerunningorwalkingonamotordriventreadmill.
2
(a) Anthropometriccharacteristics
Runners Walkers Pvalue
Age(yr) 23.7±2.4 24.6±6.9 0.70
Height(cm) 163.9±4.2 164.6±8.6 0.80
Mass(kg) 53.5±3.1 60.0±12.3 0.14
BMI(kg·m−1) 19.8±1.0 22.1±3.4 0.06
BodyFat(%) 23.0±4.9 35.7±5.2 <0.001
VO max(mL·kg−1min−1) 49.7±3.0 33.9±3.7 <0.001
2
(b) Gutpeptideconcentrationsandappetiteratingsbeforeexerciseandresttrials
Runners Walkers
Exercise∗ Rest∗ Pvalue† Exercise∗ Rest∗ Pvalue†
Ghrelin 144.7±52.6 167.8±37.0 0.33 126.8±42.8 209.4±127.8 0.09
Ghrelin 10.6±8.6 25.4±15.7 0.02 6.4±2.8 15.2±7.2 0.22
acyl
PYY 45.0±8.9 43.6±10.9 0.67 51.2±16.6 45.9±13.6 0.39
GLP-1 42.5±19.5 47.6±15.5 0.59 55.2±9.6 50.9±27.0 0.63
Hunger 8.9±9.4 13.6±16.4 0.34 7.5±9.7 17.7±28.3 0.23
Satiety 71.8±23.2 77.7±19.3 0.75 79.6±20.2 66.0±28.9 0.11
Fullness 64.6±26.4 78.2±15.6 0.29 84.2±11.4 73.6±26.7 0.20
DesiretoEat 26.6±25.1 33.4±30.1 0.51 18.4±14.2 32.4±27.8 0.04
∗Mean±SD.
†Basedonpairedt-test.
Datafrombloodsamplesaremissingforseveralparticipants before exercise and1811 ± 357kcal (14.9 ± 1.8% protein,
at one or more time points following the exercise or rest 62.3±1.8%carbohydrate,and22.7±1.5%fat)beforerest.
periods due to complications from obtaining blood via In the runners, the exercise test day fell on menstrual cycle
the indwelling catheter (i.e., occasional clotting inadequate day5.9±3.1,whereastherestdayfellonday5.2±2.9.Inthe
venous return). Data for ghrelin are missing for several walkers,exerciseandrestdaysfellon5.4±3.4and4.4±1.5,
acyl
timepointsduetoundetectablereadingsbytheRIA. respectively. Serum progesterone concentrations were less
than 2ng/mL for all participants during both exercise and
restandaveraged0.66±0.2and0.64±0.19forrunnersand
3.1. Baseline Characteristics. The characteristics of the 9 0.63±0.33and0.46±0.3forwalkersduringexerciseandrest,
runnersand10walkersaresummarizedinTable1.Table1(a) respectively,confirmingfollicularstatus.
shows that the exercise groups were fairly comparable with
respecttoageandheight.Notsurprisingly,therunnerswere
leaner than the walkers and had a higher VO max than the 3.2.OxygenUptake,HeartRateandEnergyExpenditure. Ab-
2
walkers. soluteVO ,HR,RER,RQ,RPE,andenergyexpenditure(EE)
2
Comparing exercise versus rest, Table1(b) and Figure3 duringthe60minboutofrunningorwalkingandrestalong
showunexpecteddifferencesatbaseline(preexerciseorrest) with concentrations of lactate and glucose are shown in
inmeanGhrelin onlyamongrunners,whereasmeanghr- Table2. Runners ran at an average pace of 2.9 ± 0.18m/s
acyl
elin, PYY, and GLP-1 were similar in both groups before (6.5MPH),andwalkerswalkedatanaverageof1.69±0.1m/s
exercise and rest periods. Differences in mean appetite ra- (3.77MPH). Absolute VO was higher during exercise
2
tingswerealsoobservedpriortoexerciseversusrestperiods inrunnersversuswalkers,butrelativeVO wassimilar(P =
2
amongbothrunnersandwalkers. 0.624)andaveraged70.4±4.1%and68.6±6.4%VO max
2
Theenergyandmacronutrientintakesofthecontrolled duringtherunandwalk,respectively.HRwasalso∼10bpm
dietweresimilar(P > 0.05)beforeexerciseandrestinboth higherduringexerciseintherunnerscomparedtothewalk-
the runner and walker groups. Runners averaged1868 ± ers (172bpm versus 162bpm) but was similar between the
380kcal(14.1±1.7%protein,64.8±3.2%carbohydrate,and rest trials. Energy expenditure was approximately 180kcals
21.4±2.3%fat)beforeexerciseand2035±239kcal(14±0.6% higher during exercise in runners compared to walkers
protein, 63.6 ± 1.3% carbohydrate, and 22.4 ± 1.1% fat) (483.1kcal/h versus 305.1kcal/h) but was similar at rest.
before rest. Walkers averaged1770±400kcal (14.7±1.5% Blood lactate concentration was also similarly elevated fol-
protein, 63.8 ± 2.7% carbohydrate, and 21.5 ± 2.6% fat) lowingtherunandthewalk.
6 JournalofObesity
Runners Walkers
45 45
%) 40 %) 40
crit ( crit (
o o
mat 35 mat 35
e e
h h
e e
g g
a a
er er
Av 30 Av 30
25 25
Pre 0 30 60 90 120 Pre 0 30 60 90 120
Time (min) Time (min)
Exercise Exercise
Rest Rest
(a) (b)
Figure2:Averagehematocritforrunnersandwalkersduringexercise(solidgrey)andrest(dashedblack).“Pre”representsthetimepoint
justbeforeexerciseorrest.Verticalbarsdisplaythestandarderrorofthemeanhematocritconcentrationatthattimepoint.
Table2:Oxygenuptake,energyexpenditure,andheartrateof9femalerunnersand10femalewalkersduring60minofexerciseand60min
of bed rest. VO : volume of oxygen uptake; RER: respiratory exchange ration; RQ: respiratory quotient; HR: heart rate; RPE: rating of
2
perceivedexertion.
Rest Exercise
Runners versus
Runners∗ Walkers∗ Runners∗ Walkers∗ walkeErxs † Pvalue
Ex
VO (L·min−1) 0.23±0.02 0.22±0.04 1.9±0.16 1.39±0.34 0.48(0.22,0.73) 0.001
2
RER/RQ 0.78±0.05 0.74±0.05 0.90±0.03 0.88±0.04 −0.01(−0.04,0.02) 0.570
Energyexpenditure(kcal/h) 65.5±6.7 62.3±11.5 483.1±49.7 324.6±138.1 158.5(56.2,260.7) 0.01
HR(bpm) 68.6±24.3 72.3±7.9 171.8±11.3 161.9±16.1 9.9(−4.17,24.0) 0.15
RPE — — 13.1±1.1 14.1±2.7 −0.97(−3.13,1.19) 0.35
Lactate(mmol/L) 0.76±0.26 0.92±0.4 1.4±0.66 1.0±0.55 0.4(−0.21,1.0) 0.19
Glucose(mmol/L) 5.1±0.56 5.0±0.67 6.7±1.8 5.7±0.66 1.03(−0.38,2.4) 0.14
∗Mean±SD.
†Differenceinmeans(95%confidenceinterval)fromtwo-samplet-test.
VO2:oxygenuptake;RER:respiratoryexchangeratio;RQ:respiratoryquotient;HR:heartrate;RPE:rateofperceivedexertion.
3.3.BloodConcentration,Hormones,andMetabolites Ghrelin. Figure3 (upper left panel) illustrates the average
trajectoryoveralltimepoints(onetimepointbeforeexercise
BloodConcentration. AsshowninFigure2,totalhematocrit
orrestandfivetimepointafterexerciseorrest).Averageto-
wasfairlyconstantovertimefollowingbothexerciseandrest
tal ghrelin concentration drifted upward immediately after
intherunnersandwalkers.However,becausehemoconcen-
trationwasobservedfollowingexerciseinquiteafewofthe exerciseintherunnersandthewalkers,andthenleveledoff
walkersandanoccasionaldilutesamplesfromsalineinfusion in the runners, while demonstrating large variability in the
was observed in both groups, blood data were adjusted ac- walkers. The concentration remained fairly constant after
cordingtothemethodsofDillandCostill[34]andusedin rest.Table3(a)reflectstheseresults,indicatingthatexercise
allstatisticalanalyses.Asasensitivityanalysis,werepeatedall mayincreasetheoverallrateofchangeofghrelinconcentra-
analyses using the unadjusted data and obtained similar tion in runners. While the rate of change after exercise stay
results(datanotshown). close to zero (−2.1pmol/L per minute), a positive average
JournalofObesity 7
)
b
(
d
n e e
sa alu53 44 050172188414 alu31430258
er v0. 0. 0.0.0.0.0.0. v0.0.0.0.
k P P
al
w
g
n
o ))
ngrunnersandam ff†Exerciseeect−−9.9(42.6,22.8) −1.7(2.9,6.3) −−−6.7(13.2,0.14−−−16.5(28.0,5.0−0.60(2.9,4.1)−3.2(1.6,8.0)−−0.35(3.9,3.2)−−1.9(4.4,0.67) ff†Exerciseeect−68.0(70.0,205.9)−−6.3(23.0,10.3)13.3(1.9,24.7)−8.7(23.8,41.2)
mo ers
k
orafterrest,a rs∗Rest..−±46232 ..−±1347 ..−±2217..±69181..±7645..−±7638..−±6650..±8337 Wal∗Rest..±2871519..±40205..−±36132..±11105
se ke −
ci al
r W
e
x
e 6 6
minutesafter nts ∗Exercise..−±12833 ..±1742 ..−±9483..−±10210..±9249..−±5668..−±8243..±7944 ∗Exercise..±3921254..−±2353..±98184..±98365
ngerratingsover120=0).(att exerciseoveralltimepoi Pvalue0.12 0.56 0.0410.0020.150.230.0420.37 ffmediateeectofexercise Pvalue0.760.0750.0080.022
ffable3:Eectofexerciseon(a)rateofchangeofgutpeptideconcentrationsandhuutpepetideconcentrationsandhungerratingsimmediatelyafterexerciseorafterrest ff(a)Eectof Runnersff∗∗†RestExerciseeectExercise....±−±−Ghrelin(pmol/L)1002292111712.9(3.9,29.7)Ghrelin....acyl±−±−3610014392.9(7.6,13.4)(pmol/L)....−±−±−−−PYY(pmol/L)392417162.0(4.0,0.095)....−±±−−−GLP-1(pmol/L)8579156310.7(17.0,4.4)...±±−Hunger1345910463.6(1.5,8.7)....−±−±−−Satiety877882762.6(7.1,1.8)....−±−±−−−Fullness1066493333.9(7.7,0.16)....±±−DesiretoEat1026384431.9(2.4,6.1)∗±MeanSDofslopes.†ffEstimatedeect(95%confidenceinterval)fromlinearregression,adjustingforbaseline. (b)Im Runnersff∗∗†RestExerciseeectExercise....−±±−−Ghrelin(pmol/L)37711364357.3(57.2,42.6)....±±−Ghrelin(pmol/L)7957003927.9(0.9,16.7)acyl....±−±PYY(pmol/L)83127405812.3(3.6,21.0)....±−±GLP-1(pmol/L)3032552218932.4(5.3,59.5)∗fft±MeanSDofdierenceinandbaseline.0†ffEstimatedeect(95%confidenceinterval)fromlinearregression.
Tg
8 JournalofObesity
Total ghrelin Ghrelinacyl
Runners Walkers Runners Walkers
mol/L) 250 mol/L) 250 mol/L) 50 mol/L) 50
Average total ghrelin (p 125000 Pre 0 30 60 90 120 Average total ghrelin (p 125000 Pre 0 30 60 90 120 Average acyl-ghrelin (p 123400000 Pre 0 30 60 90 120 Average acyl-ghrelin (p 123400000 Pre 0 30 60 90 120
Time (min) Time (min) Time (min) Time (min)
PYY GLP-1
Runners Walkers Runners Walkers
L) 80 L) 80 L) 100 L) 100
mol/ 70 mol/ 70 mol/ 80 mol/ 80
p p p p
Y ( 60 Y ( 60 1 ( 1 (
Average PY 345000 Average PY 345000 Average GLP- 246000 Average GLP- 246000
Pre 0 30 60 90 120 Pre 0 30 60 90 120 Pre 0 30 60 90 120 Pre 0 30 60 90 120
Time (min) Time (min) Time (min) Time (min)
Exercise Exercise Exercise Exercise
Rest Rest Rest Rest
Figure3:Averagechangeinghrelin(pmol/L,upperleftpanel),ghrelin (pmol/L,upperrightpanel),PYY(pmol/L,lowerleftpanel),and
acyl
GLP-1(pmol/L,lowerrightpanel)forrunnersandwalkersduringexercise(solidgrey)andrest(dashedblack).“Pre”representsthetime
pointjustbeforeexerciseorrest.Verticalbarsdisplaythestandarderrorofthemeanconcentrationofgutpeptideatthattimepoint.
postexerciseslope(10.0pmol/Lper30minutes)andanover- shows evidence of the effect of exercise on the rate of cha-
allpositivedifferencebetweenexerciseandrest(12.9pmol/L ngeofPYY,withexercisecausingafasterdeclineinPYYcon-
per minute, 95% CI [−3.9, 29.7], P value= 0.12) are esti- centration over time among runners (−2.0pmol/L per 30
mated.Meanwhile,forwalkers,thelargervariabilityatlater minutes, 95% CI [−4.0, −0.095], P value = 0.041) and
timepointsmayobscurethetrueeffectofexercise.Table3(b) among walkers (−6.7pmol/L per 30 minutes, 95% CI
containsresultsofexploratoryanalysisrelatingtoimmediate [−13.2,−0.14],P value=0.43),althoughtheeffectwasnot
effects of exercise. Figure3 (upper right panel) shows pat- statisticallysignificantinthewalkerspotentiallyduetohigh
ternsforaverageGhrelin concentrationthataresomewhat variability.Immediateeffectswerealsoevident,butpositive
acyl
similartothosefortotalghrelin.Table3(a)showslittleevi- (Table3(b)), thus reflecting the observed pattern of an im-
denceofanexerciseeffectontherateofchangeofGhrelin mediate rise in concentration followed by a decline among
acyl
concentrationovertime.Thereissomeindication,however, bothrunnersandwalkers.ThepositiveAUCforPYYtended
of a larger immediate increase in Ghrelin concentration tobehigherafterexerciseversusrestintherunners.Negative
acyl
after exercise versus after rest among runners (7.9pmol/L, AUCwasalsofoundtobehigherafterexerciseversusrestin
95%CI[−0.9,16.7],Pvalue=0.075). walkers(Table4).
The positive AUC (area above baseline) for both total SimilartoPYY,GLP-1concentrationpeakedimmediately
ghrelinandghrelin wasfoundtobehigherfollowingex- afterexerciseinbothrunnersandwalkersreturningtopre-
acyl
ercise in the runners but not the walkers. Negative AUC exercise concentrations at approximately 30min after exer-
(areaunderbaseline)wasfoundtobesmallerfollowingex- cise. Unlike PYY, GLP-1 dipped visibly below baseline after
ercise.Together,theseresultsindicatedthattotalresponseas 60min after exercise in both groups (Figure3). Table3(a)
measuredbytotalghrelinandghrelin tendedtobehigher showsfairlylargeeffectsofexerciseontherateofchangeof
acyl
afterexercisethanafterrestamongrunners(Table4). GLP-1. Again, exercise caused a faster decline in GLP-1
concentration among both runners (−10.7pmol/L per 30
minutes,95%CI[−17.0,−4.4],P value=0.002)andwalkers
PYYandGLP-1. Inrunners,PYYconcentrationpeakedim- (−16.5pmol/Lper30minutes,95%CI[−28.0,−5.0],P va-
mediately after exercise (Figure3) then gradually returned lue = 0.008). There was evidence of an immediate effect of
to baseline over the 120min after exercise; whereas in wa- exercise among runners, but not in walkers. The positive
lkers, PYY concentration peaked at 30min after exercise AUC for GLP-1 was not different following exercise com-
beforereturningtobaseline90minafterexercise.Table3(a) pared to rest in either the runners or the walkers, however,
JournalofObesity 9
Table4:EffectofexerciseonAUCvaluesforhormonesandmetabolites.ResultsforbothpositiveandnegativeAUCarepresented.
Hormone/ Runners Walkers
P
metabolite Exercise∗ Rest∗ Exerciseeffect† Exercise∗ Rest∗ Exerciseeffect† Pvalue
value
Ghrelin
(+)area 20641±16238 6322±6450 14319(340,28298) 0.05 18157±26247 6863±9390 11294(−10486,33075) 0.27
(−)area 5672±16471 3908±7977 1764(−12808,16336) 0.79 6839±8708 24574±32687 −17734(−44816,9348) 0.17
Ghrelin
acyl
(+)area 6246±4933 700±584 5546(1822,9271) 0.01 2067±2437 1345±1575 723(−833,2279) 0.32
(−)area 105±183 1688±2184 −1583(−3172,6) 0.05 813±1671 946±1283 −133(−1297,1031) 0.80
PYY
(+)area 1796±2667 59±92 1737(−290,3764) 0.08 90±163 1073±2325 −983(−2686,719) 0.22
(−)area 2575±2306 4211±3103 −1635(−4678,1407) 0.25 6912±6575 2415±1483 4497(−502,9496) 0.07
GLP-1
(+)area 1114±926 693±691 421(−313,1155) 0.22 556±650 656±618 −181(−851,488) 0.54
(−)area 802±789 941±1154 −139(−1273,995) 0.78 1957±2058 1447±3459 1658(4,3311) 0.05
∗Mean±SDofAUC.
†Differenceinmeans(95%confidenceinterval)frompairedt-test.
Table5:Effectofexerciseonabsoluteenergy,relativeenergy,andmacronutrientintake,amongrunnersandamongwalkers.
Runners Walkers
Exercise∗ Rest∗ Exerciseeffect† Pvalue Exercise∗ Rest∗ Exerciseeffect† Pvalue
Absolute
energyintake 485.8±183.4 480.4±126.4 5.5 0.917 623.9±139.1 550.6±162.4 73.2 0.08
(−112.0,122.9) (−11.0,157.5)
(kcals)
Relative
energyintake −193.9±205.8 283.8±120.6 −477.7 <0.001 126.8±195.8 366.0±183.6 −274.6 <0.001
(−610.1,−345.3) (−385.0,−164.3)
(kcals)
Protein(g) 19.3±6.0 19.3±4.7 −0.046 0.980 27.6±7.3 24.2±9.5 3.4 0.05
(−4.1,4.1) (0.043,6.8)
Carbohydrate 80.5±37.4 79.0±20.9 1.5 0.877 88.6±28.5 83.1±22.2 5.5 0.51
(g) (−20.6,23.7) (−13.0,24.0)
Fat(g) 11.0±3.5 11.3±5.4 −0.38 0.830 19.2±5.8 15.1±7.4 4.1 0.001
(−4.3,3.6) (2.2,6.0)
∗Mean±SD.
†Differenceinmeans(95%confidenceinterval)frompairedt-test.
the area below baseline was greater in the walkers (1957± significantlydifferentafterexerciseversusafterrestforeither
2058and1447±3459,P = 0.05)butnottherunnersafter group.
exerciseversusrest(Table4).
3.5.AdLibitumFoodIntake. AsshowninTable5,therewas
3.4. Hunger and Satiety Ratings. As shown in Figure4 (top no evidence of a difference between absolute energy intake
panel),ratingsof“hunger”increasedfrombaselineacrossthe and macronutrient intake at the free-choice meal following
120minafterexerciseorafterrestperiodinboththerunners running versus rest. However, absolute intake tended to be
andwalkersduringtheexerciseandresttrials.Similarresults higher following walking compared to rest (73.2kcals, 95%
wereobservedfordesiretoeat,thatis,howmuchyouthink CI [−11.0, 157.5], P value= 0.080). Interestingly, walkers
you can eat (data not shown). Ratings of satiety (Figure4, (butnotrunners)tendedtoconsumemoreprotein(inwal-
bottom panel) and fullness (data not shown) tended to kers: 3.4g, 95% CI [0.043, 6.8], P value= 0.048) and fat
decrease from baseline across the 120min after exercise or (inwalkers:4.1g,95%CI[2.2,6.0],P value=0.001)follow-
after rest period in both groups during both trials. We see ingexercisecomparedtorest(Figure5).
from Table5 that there was not enough evidence to show
aneffectofexerciseontherateofchangeovertimeforany 3.6.RelativeEnergyIntake. Afteradjustingforthecostofex-
of the four subjective appetite ratings in either group. The ercise or rest, relative energy intake was lower following
AUCsforthefourappetiteratingswerealsonotfoundtobe exercise compared to rest in both groups (P 0.001). In
10 JournalofObesity
Hunger
Runners Walkers
100 100
80 80
ng 60 ng 60
ati ati
e r e r
g g
a a
Aver 40 Aver 40
20 20
0 0
Pre 0 30 60 90 120 Pre 0 30 60 90 120
Satiety
Runners Walkers
100 100
80 80
ng 60 ng 60
ati ati
e r e r
g g
a a
ver 40 ver 40
A A
20 20
0 0
Pre 0 30 60 90 120 Pre 0 30 60 90 120
Exercise Exercise
Rest Rest
Figure4:Averagechangeinhunger(upperpanel)andsatiety(lowerpanel)forrunnersandwalkersduringexercise(solidgrey)andrest
(dashedblack).“Pre”representsthetimepointjustbeforeexerciseorrest.Verticalbarsdisplaythestandarderrorofthemeanforhunger
andsatietyatthattimepoint.Dataforfullnessanddesiretoeatarenotshown.
runners,relativeenergyintakewas477.7kcalslower(95%CI satiety and fullness and negatively associated with hunger
[−610.1,−345.3])afterexercisecomparedtoafterrest.The and desire to eat. In the walkers, there may be some indi-
difference was smaller in walkers, with after exercise being cation of an association between hunger ratings and Ghre-
274.6kcalslower(95%CI[−385.0,−164.3])thanafterrest. lin (0.63units,95%CI[−0.19,1.46],P value=0.12)and
acyl
GLP-1(0.095units,95%CI[−0.32,0.028],P value=0.095)
concentrations.
3.7. Gut Peptides and Appetite Ratings. In the runners, the
change in concentrations of PYY and GLP-1 was predictive 4.Discussion
ofthechangeinhunger(Table6).Analogousresultswereob-
tainedforsatiety,fullness,anddesiretoeat(datanotshown). Thepurposeofthecurrentstudywastoevaluatetheeffectof
IncreasesinPYYandGLP-1werepositivelyassociatedwith 60minofmoderatelyhardrunningandwalkingatthesame