Armele
Dornelas
de
Andrade
a,∗∗aDepartmentofPhysicalTherapy,UniversidadeFederaldePernambuco—UFPE,Recife,Brazil
bDepartmentofRespiratoryTherapyLewisSchoolofNursingandHealthProfessions,GeorgiaStateUniversity,Atlanta,GA,USA cDipartimentodiElettronica,InformazioneeBioingegneriaPolitecnicodiMilano,Milan,Italy
a
r
t
i
c
l
e
i
n
f
o
Articlehistory: Received2April2015 Receivedinrevisedform 18December2015 Accepted11February2016 Availableonline18February2016 Keywords: Breathingpattern Opto-electronicplethysmography Aging Respiratorymechanics
a
b
s
t
r
a
c
t
Itisnotcompletelydescribedhowagingaffectventilatorykinematicsandwhatarethemechanisms adoptedbytheelderlypopulationtoovercomethesestructuralmodifications.Giventhis,theaimwasto evaluatetheacuteeffectsofdifferentinspiratoryeffortsonventilatorypatternandchestwall compart-mentaldistributioninelderlywomen.Variablesassessedincluded:tidalvolume(Vt),totalchestwall volume(Vcw),pulmonaryribcage(Vrcp%),abdominalribcage(Vrca%)andabdominalcompartment (Vab%)relativecontributionstotidalvolume.Thesevariableswereassessedduringquietbreathing, max-imalinspiratorypressuremaneuver(MIP),andmoderateinspiratoryresistance(MIR;i.e.,40%ofMIP). 22youngwomen(age:23.9±2.5years)and22elderlywomen(age:68.2±5.0years)participatedtothis study.Itwaspossibletoshowthatduringquietbreathing,Vab%waspredominantinelderly(p<0.001), inyoung,however,Vab%wassimilartoVrcp%(p=0.095).DuringMIR,Vrcp%waspredominantinyoung (p<0.001)andcomparabletoVab%inelderly(p=0.249).WhenMIPwasimposed,bothgroupspresented apredominanceofVrcp%.Inconclusion,therearedifferencesinabdominalkinematicsbetweenyoung andelderlywomenduringdifferentinspiratoryefforts.Inelderly,duringmoderateinspiratoryresistance, thepatternisbeneficial,deep,andslow.Although,duringmaximalinspiratoryresistance,theventilatory patternseemstopredictimminentmusclefatigue.
©2016ElsevierB.V.Allrightsreserved.
1. Introduction
Withagingrespiratorymusclesperformancedecreasesdueto
sarcopeniaandchangesinmusclefibers(Lalley,2013)decreasing
maximal strength development (Williams et al., 2002).
Addi-tionally,as a consequence of the calcificationof costovertebral
cartilagesandjoints,intercostalspacesandthoracic compliance
arereduced(Rossietal.,2008).
Allthesechangesmightaffectventilatorykinematics;however,
theadaptivemechanismsadoptedtoovercomethesestructural
changesintheelderlypopulationarestillnotcompletely
under-∗ Correspondingauthor.Fax:+558121268491. ∗∗ Correspondingauthor.
E-mailaddresses:[email protected]
(H.MunizdeSouza),[email protected]
(T.Rocha),[email protected](S.L.Campos),[email protected]
(D.C.Brandão),fi[email protected](J.B.Fink),[email protected]
(A.Aliverti),[email protected](A.D.deAndrade).
stood.It´ıs mandatorytodifferentiate thephysiological changes
inducedbyagefrompathologicalchanges.
The chest wall kinematics evaluation using opto-electronic
plethysmography(OEP)hasemergedasausefulmethodtoevaluate
thechangesgeneratedindifferentsituations(Paisanietal.,2013;
Wilkensetal.,2010).TheOEPrecordseachrespiratorycycleinreal
timemakingitpossibletoevaluatetheventilatorypatternandthe
chestwallvolumewithitscompartmentaldistribution(pulmonary
ribcage,abdominalribcageandabdomen)(Parreiraetal.,2012).
However,studiesthatobservedtheeffectsofsenescenceoverchest
wallkinematicsusingtheOEP(Brittoetal.,2009)arestillscarce.
Moreover,thechangesgeneratedin differentinspiratory efforts
havenotbeenevaluatedyet.
Wehypothesizedthatelderlydevelopdifferentchestwall
kine-maticandventilatorypatterns,comparedtoyoung,whentheyare
submittedtodifferentinspiratoryloads.Intheelderlypopulation,
this differencewould bemore noticeableintheabdominal
vol-umecontributionsince,duetosenilesarcopenia,thedecreasein
respiratory musclestrength wouldimpairthecapacity to
over-come upperchest wallrestrictive forces.Considering that after
http://dx.doi.org/10.1016/j.resp.2016.02.004
Fig.1.Maximalinspiratorypressureassessmentduringopto-electronicplethysmographyevaluation(left)andthree-dimensionalmodelofribcagecompartments. Pul-monaryribcage(Rcp),abdominalribcage(Rca),andabdomen(Ab)(right).
menopausewomen havelower levelsof estrogenand that this
intensifies thesenilesarcopenia(Kenny etal., 2003), theaging
relatedchangesinchestwallkinematicsmightbemoreevident
inthisgender.Giventhis,wedecidedtotestourhypothesisina
groupformedexclusivelybywomen.Therefore, theaimwasto
evaluatetheacuteeffectsofdifferentinspiratoryeffortson
venti-latorypatternandchestwallcompartmentaldistributioninelderly
women.
2. Methods
2.1. Studydesign
Thiswasacross-sectionalstudyapprovedbytheResearchEthics
CommitteeoftheCenterforHealthSciencesattheFederal
Uni-versityofPernambuco(CEP/CCS/UFPENo457/11).Theresearch
wasconductedintheLaboratoryofCardiopulmonary
Physiother-apy,DepartmentPhysiotherapy,FederalUniversityofPernambuco
(UFPE)fromAugusttoDecember2014.Allvolunteerssignedafree
andinformedconsentform.
2.2. Participants
Thesamplewasformedby22 elderlywomenand22 young
women.Apilotstudywasmadewithfiveindividualsineachgroup
tocalculatethesample.Atotalof34participantswouldprovide
95%powerand alphalevelof0.05todetectdifferencebetween
groupsinthepulmonaryribcagecontribution.Thefollowing
inclu-sioncriteria were adopted: agebetween20 to 80 years;tobe
able towalk without assistance; to have cognitive integrity in
theelderlygroup,assessedbytheMini-MentalStateExamination
(MMSE).Theexclusioncriteriawere:contraindicationordifficulty
toperformtheevaluationprocedures;respiratorymusclestrength
lower than 70% of the predict (Neder et al., 1999); smoking;
hemodynamicinstability;neuromusculardegenerative diseases;
pulmonarycomorbidities;heartdiseaseandusersofmedications
thatchangethebonemetabolismorthemusclestrength.
2.3. Datacollection
Allvolunteerswereinitiallysubmittedtoananthropometric,
clinical,anddemographicevaluation.Thelevelofphysical
activ-ity was evaluated through a self-reported instrument adapted
totheBrazilianpopulation,theProfileofHumanActivity (PHA)
(Souzaetal.,2006).Thisinstrumentquantifiesthelevelofphysical
activitythroughtheadjustedactivityscore(AAS)sortingthe
indi-vidualintothreecategories:inactive(AAS<53),moderatelyactive
(53≤AAS≤74),andactive(AAS>74).Afterwards,thevolunteers
wereinstructedtobreathewithamoderateinspiratoryresistance,
toensurethecorrectperformanceofthetechniqueseveraldays
beforethemeasurements.Theevaluationwasconductedintwo
stages.Inthefirst,weassessedpulmonaryfunctionandmaximal
respiratorypressures.Inthesecond,ventilatorypatternandchest
wallcompartmentaldistributionwereassessedbytheOEP.
2.3.1. Pulmonaryfunctiontests
Testswereperformedusingaportablespirometer(Micro
Med-ical,Microloop,MK8,England).Thehighestvalueinforcedvital
capacity (FVC), forced expiratoryvolumein one second (FEV1),
forcedexpiratoryflow25–75%(FEF25–75%),andtheFEV1/FVCratio
wasused,afterthreeacceptablemaneuvers.Referencevaluesfor
Brazilianadultpopulationwereconsidered(Pereiraetal.,2007).
2.3.2. Maximalrespiratorypressures
Themeasurementofthemaximuminspiratorypressure(MIP)
andmaximumexpiratorypressure(MEP)wasperformedusinga
digitalmanometer(MVD300,Globalmed,Brazil)fromresidual
vol-umeandtotallungcapacity,respectively(Nederetal.,1999).At
leastfivemeasurementswerecarriedoutuntilthreeacceptableand
reproduciblemeasurementswereobtained,i.e.,withoutair
leak-ageandwithlessthan10%differenceamongthem,withthehighest
valueobtainedbeingregistered(EvansandWhitelaw,2009).
2.3.3. Breathingwithmoderateinspiratoryresistance(MIR)
The moderateinspiratory resistancewasperformedwithan
inspiratorymuscletrainingdevice,theThreshold®IMT
(Respiron-ics,NJ,USA),commonlyusedtotrainhealthypeople(Downeyetal.,
2007;EnrightandUnnithan,2011)aswellasotherspopulations (Gosselinket al.,2011;Plentzetal., 2012).Thevolunteers
per-formedtheMIRinaseatedpositionandwereorientedtobreathe
quietlyandkeeparegularrespiratoryratepriortothetest.
Dur-ingtheevaluation,therewasnoincentiveorverbalinstructionsto
thevolunteers.Thedevicewascoupledtothevolunteerthrougha
mouthpiecethatprovidesalinearresistiveload(DeAndradeetal.,
2005)establishedat40%ofthepreviouslyobtainedMIP.Nasalclips
werealsousedduringMIR.ThedurationoftheMIRsessionwas
threeminutes(Souzaetal.,2014).Duringexpiration,therewasno
Vrca%MIR 22.6±5.5 24.7±12.3 0.639 Vab%MIR 31.1±13.5 40.2±13.7 0.046 VcwMIP(L) 19.3±3.2 25.9±5.2 <0.001 Vrcp%MIP 55.0±3.9 50.0±4.9 0.003 Vrca%MIP 15.5±2.5 16.4±2.4 0.197 Vab%MIP 29.5±3.1 33.6±4.3 0.002
BMI:bodymassindex;HAP:humanactivityprofile;FEV1:forcedexpiratoryvolumeinthefirstsecond;FVC:forcedvitalcapacity;FEF25–75:forcedexpiratoryflow25%e 75%;MIP:maximalinspiratorypressure;MEP:maximalexpiratorypressure;QB:quietbreathing;MIR:moderateinspiratoryresistance;Vt:tidalvolume;Vcw:chestwall volume;Vrcp%:pulmonaryribcagecontributionvolume;Vrca:abdominalribcagecontributionvolume;Vab:abdominalcontributionvolume.
2.3.4. Opto-electronicplethysmography(OEP)
TheOEP(BTSBioengineering,Milano,Italy)wasusedtoassess
theventilatorypatternandthechestwallcompartmental
distri-bution.Eighty-ninereflectivemarkerswereplaced accordingto
anatomical referencesand attached to thetrunk of volunteers
seatedwithoutabackrestwithhypoallergenicadhesive(Aliverti
andPedotti,2005).
Eightinfraredcameras(fourinfrontandfourbehindthe
vol-unteers)tracedthethree-dimensionalcoordinatesofthereflective
markersastheymovedandthedevicesoftwarecalculatedthechest
wallvolume(Vcw)throughsurfacetriangulation(Brandãoetal.,
2012).Thechestwallcompartmentaldistributionwascomposedof
threecompartments:pulmonaryribcage(Vrcp—portionoftherib
cageincontactwiththelungs),abdominalribcage(Vrca—portion
oftheribcageopposed tothediaphragm),and abdomen(Vab)
(Parreiraetal.,2012)(Fig.1).
The chest wall compartmental distribution was assessed in
threedifferentconditions:(a)during3minofquietbreathing(QB);
(b)during3minwithmoderateinspiratoryresistance(MIR);(c)
whileperforming2 maneuversof maximalinspiratorypressure
(MIP)(Fig.1).TheventilatorypatternwasevaluatedduringtheQB
andMIR.Thedatawasassessedwith5minrestbetweeneach
con-ditions.DuringQBandMIR,thefollowingvariableswereassessed:
tidalvolume(Vt),chestwallvolumecompartmentaldistribution
(Vrcp%,Vrca%andVab%),respiratoryrate(RR),inspiratorytime(Ti),
expiratorytime(Te),totalrespiratorycycletime(Ttot),andworkof
breathing(WOB).DuringMIP,chestwalltotalvolumeandits
com-partmentaldistributions(Vrcp%,Vrca%andVab%)wereevaluated.
2.4. Statisticalanalysis
The sample characteristics and statistical analysis of the
datawereexpressedas meanand standarddeviation (SD).The
Shapiro–Wilktestwasusedtoevaluatethenormalityofthedata.
Differences between controls and elderly women were
evalu-ated by the Mann–Whitney test. The comparison between the
ventilatorypatterninQBand MIRwasdonewiththeWilcoxon
test.Tocomparethepercentageofthecontributionofthe
com-partments in each situation (QB, MIR or MIP) and between
situations (QB×MIR×MIP), we used the nonparametric
Fried-mantest.Wherestatisticalsignificancewasfound,thedifferences
amongthedatawereevaluatedusingtheWilcoxontest.The
Spear-mancorrelationtestwasusedtoevaluatetherelationshipbetween
ageandventilatoryvariables.Theanalysiswasconductedusing
theprogramSPSSforWindows(version20.0,Chicago,IL)anda
significancelevelofp<0.05wasestablished.
3. Results
The study included 22 elderly women and a control group
with22 youngwomen(Fig.2).Anthropometricdata,
spiromet-ricvariables,respiratorymusclestrength,levelofphysicalactivity
(evaluatedthroughPHA),totalvolumes,andchestwall
compart-mentaldistributionareinTable1.Thecontrolgroupdidnotuse
medications.Intheelderlygroup,tenvolunteers(45%)used
med-icationsforhypertensioncontrol,three(14%)fordiabetescontrol,
two(9%)forboth,andsevenvolunteers(32%)didnotuse
medica-tions.
Thepatternventilatoryvariablesintheelderlyandthecontrol
groupsduringtheQBandMRIwereexposed inTable2.During
MIR,theventilatorypatternshowedchangescomparedtoQBin
bothgroups.
Thecomparisonofchestwallvolumecompartmental
distribu-tion(Vrcp%,Vrca%andVab%)ineachsituation(QB,MIRorMIP)is
showninFig.3.WeobservedthatintheQB,theVab%was
predomi-nantinelderlywhileVrcp%andVab%weresimilarincontrolgroup.
InbothgroupsduringtheMIR,theVrcp%predominated,followed
byVab%andVrca%.IntheMIP,theVrcp%increasedinbothgroup.
In the comparison of each chest wall compartment (Vrcp%,
Vrca% and Vab%) between situations (QB×MIR×MIP), we
observedthatthebehaviorwassimilarinbothgroups.TheVrcp%
increasedduringMRIandMIPinrelationtoQB.TheVab%decreased
whentheinspiratoryeffortwasmajor(MIRandMIP)whileVrca%
increaseduringtheMIRbutdecreasedintheMIP.
Theageshowedsignificative(p<0.05)correlationwith:Vt,QB
(r=−0.524), Vrcp%,QB (r=−0.585), Vab%,QB (r=0.585), Ttot,QB
Fig.2.Flowchartofparticipants.
Vt,MIR (r=0.407), Vrcp%,MIR (r=−0.307), Ti,MIR (r=0,324),
WOB,MIR(r=0.034),Vcw,MIP (r=0.596), Vrcp%,MIP(r=−0.391)
andVab%,MIP(r=0,457).Therewerenocorrelationsbetweenage
andothersvariables.
4. Discussion
Tothebestofourknowledge,thisisthefirststudythat
evalu-atestheventilatorykinematicsinelderlyduringthreeprogressive
Fig.3. Comparisonbetween pulmonaryrib cage(Vrcp%),abdominal ribcage (Vrca%),andabdominal(Vab%)contributionsineachsituation:quietbreathing (QB),breathingwithmoderateinspiratoryresistance(MIR),andmaximal inspira-torypressuremeasurement(MIP).(Graphrepresentedasmeanandstandarderror. *p<0.05,**p<0.01and***p<0.001;Wilcoxontest).
revealedthatduringQB,Vab%ispredominantintheelderly,while
inyoungwomen,Vrcp%prevails.Furthermore,ventilatorypattern
changeswhenmoderateinspiratoryloadsareadded.Therewere
differences onchestwallvolumedistributionfrom QBto
max-imalinspiratoryefforts.Although,despitethedifferences inthe
chestwallvolumedistribution,bothgroupsbehavedsimilarly
dur-ingtheincreaseininspiratoryresistance.Weobservedamoderate
correlationbetweenage,Vrcp%,andVab%duringtheQB.
Sincehealthyindividualswithoutpreviousclinicallimitations
formedbothgroups,itwaspossibletocomparetheirbaseline
val-uesandalldifferencesobservedmightberestrictedtotheaging
process(Table1).
DuringQB,Vab%waspredominantintheelderlygroupbut
sim-ilartotheVrcp%inthecontrolgroup.Ourfindingsagreewiththe
reportsofBrittoetal.(2009)whereabdominalcontributionwas
prevalentinelderlysubjectsduringQB(Brittoetal.,2009).The
decline ofchestwallmovementdue totheaging process(Berg
etal.,2012)isreinforcedinourstudy,wherearelationshipwas
foundbetweenageanddecreasedtidalvolumeandVrcp%,aswell
aswithanincreasedVab%.Thissuggeststhatabdominal
contribu-cleactivityofthelowerribcageandthelungventilationinthe
middlethirdwhilemoderateinspiratoryloadswereset.
Althoughwedidnotfindpreviousliteratureinelderly
popula-tion,ourresultsreinforcethehypothesisthatthedecreaseofthe
chestwallcompliancealtersthevolumedistributionandmoderate
inspiratoryeffortsareinsufficienttoovercometheresistiveforces
oftheupperchestwall.However,thehealthyelderlypresented
a similarventilatorybehaviorcompared toyoungvolunteersin
theseconditions.Thissuggeststhatduringsenescenceventilatory
behaviorinmoderateeffortsremainsthesamedespiteallparticular
structuralchanges(Lalley,2013).
In thepresentstudy,itwaspossibletoobservethat
respira-torypatternchangesinbothgroupsduringtheMIR(Table2).This
suggeststhat breathingbecomes deeperand slowerin orderto
overcometheresistanceimposed.Moreover,despitetheincreased
work ofbreathing, ventilatory pattern adoptedduring MIR
dif-fered from respiratory muscles fatigue prediction model (Berg
etal.,2012;Phillipsetal.,2015).Inthismodelthebreathingoften
becomesrapidandsuperficial(Hostettleretal.,2011).Ourresults
suggestthat changesintheventilatorypatternsand ventilatory
kinematicsduringMIRintheelderlymightbeabeneficial
venti-lationstrategy.Thus,wereinforcetheideathattheapplicationof
exerciseprotocolsandactivitiesthatrequiremoderateinspiratory
effortscanbesafelyperformedinthispopulation.
WhenthevolunteerswereevaluatedduringMIP,Vrcp%
pre-vailedinbothgroups.However,theincreaseinVrcp%intheelderly
groupoccurredwithadecreaseinVab%.Meanwhile,inthecontrol
group,thehighervaluesofVrcp%happenedduetoadecreasein
Vrca%andVab%,comparedtoQB(Fig.3).
Table2
Ventilatorypatternchangesbetweenquietbreathing(QB)andbreathingwith mod-erateinspiratoryresistance(MIR)inbothgroups.
Variables QB MIR Pvalue
VtEG(l) 0.4±0.1 1.3±0.5 <0.001 VtCG(l) 0.6±0.2 0.9±0.5 0.035 RREG(ipm) 18.5±4.4 11.8±6.3 <0.001 RRCG(ipm) 14.2±3.6 12.9±4.1 0.372 TtotEG(s) 3.5±0.8 7.0±4.0 <0.001 TtotCG(s) 4.6±1.2 5.4±1.9 0.101 TiEG(s) 1.4±0.4 4.4±2.8 <0.001 TiCG(s) 2.0±0.6 2.9±1.3 0.003 TeEG(s) 2.1±0.5 2.6±1.6 0.527 TeCG(s) 2.6±0.8 2.5±1.0 0.123 WBEG 41.0±4.4 61.8±9.5 <0.001 WBCG 42.1±4.4 61.8±9.5 <0.001
QB:quietbreathing;MIR:moderateinspiratoryresistance;EG:elderlygroup;CG: controlgroup;Vt:tidalvolume;RR:respiratoryrate;Ttot:totalrespiratorycycle time;Ti:inspiratorytime;Te:expiratorytime;WB:workofbreathig;l:liters;s: seconds;ipm:incursionsperminute.
TheMIPmaneuverisperformedwithamaximalisometric
con-tractionofdiaphragmmusclewithoutvolumechange(Cohnetal.,
1997).Giventhis,whenthesubjectsareundermaximal
respira-toryefforts,accessoryrespiratorymusclesmighthavetoovercome
chestwallstiffnessandthiscouldbethereasonforanincreased
Vrcp%.However,intheelderly,theincreaseinVrcp%occurredwith
adecreaseinVrca%andVab%.ItisknownthatVab%ishighlyrelated
todiaphragmmobility(AlivertiandPedotti,2005;Illietal.,2011).
Therefore,wehypothesizethatagainsthighrespiratoryresistances,
theelderlypresentsadecreasedactivationofdiaphragmmuscle
(i.e.,lowerVrca%)aswellasadecreaseddiaphragmmobility(i.e.,
lowerVab%).Accordingtothisbehavior,theelderlymightbemore
vulnerabletoventilatorymusclefatiguewhenmaximaleffortsare
required.Thisreinforcestheneedtoestablishspecific
therapeu-ticstrategiesforthepreventionofsenilemuscleweaknesssince
maximaleffortswillbenecessaryinextremesituations.After
per-formingaprotocolofnormocapnichyperpneainhealthyadults,Illi
etal.(2013)observedadecreaseinVab%startingfromthemiddle
ofthetest,withasimultaneousincreaseinVrcp%andreductionof
theendinspiratoryvolumesuggestingimpendingfatigueofcostal
inspiratorymuscles.Thus,thisstudysuggeststhattheventilatory
kinematicsobservedduringmaximalefforts shouldnotbe
per-formedforlongperiods,sinceitscontinuitymightpredisposeto
thedevelopmentofrespiratorymusclefatigue.
TheincreaseinVrca%duringMIRandVcrp%duringMIPinboth
groupssuggestthat, dependingontheintensityof thenegative
pressuregenerated, thelung volumecanbeshiftedtospecifics
segments,which maybeuseful toimplementing techniquesof
selectivepulmonaryre-expansion.However,itisstillnecessaryto
understandtheimpactofthisventilatorybehaviorduring
max-imum inspiratory efforts in the clinical practice. Thus, at this
moment,treatmentprotocolsthatrequireexhaustiveinspiratory
workshouldstillbeindicatedwithcautioninelderlypatients.
4.1. Limitations
Itwasnotpossibletostratifythestatisticalanalysisbyneither
age(i.e.,60–69yearsandabove69years)neitherbyBMI(i.e.,<18;
18–24;>24),inordertounderstandtherelationshipofthese
sub-groupstochestwallvolumecompartmentaldistributionduetothe
baselineheterogeneitybetweengroups.Despitethis,ourresearch
contributedtoexploitthepeculiaritiesofventilatorypatternand
thoracoabdominalkinematicsduringdifferentinspiratoryefforts
inelderlywomen.
5. Conclusion
Thepresentstudyshowedthattherearedifferencesbetween
youngandelderlyventilatorykinematicsduringinspiratoryefforts.
However,wealsofoundthatbothgroupshaveasimilar
ventila-torybehaviorastheinspiratoryeffortresistanceincreases.During
moderateefforts,theventilatorypatternisbeneficialwithslowand
deepbreaths.However,whenhighresistanceisimposed,the
ven-tilatorybehaviorseemstopredictimminentmusclefatigue.Given
this,inordertoadoptsaferexerciseprotocolstothisagegroup,
theserespiratorydifferencesmustbeconsidered.
Acknowledgments
This research was supported by grant: FACEPE APQ 0821
4.08/08,CNPq:Proc482069/2012-0andPVE400801/2013-2.
References
Aliverti,A.,Pedotti,A.,2005.Opto-electronicplethysmography.MonaldiArch. ChestDis.59,12–16.
Berg,K.M.,Lang,G.R.,Salciccioli,J.D.,Bak,E.,Cocchi,M.N.,Gautam,S.,Donnino, M.W.,2012.Therapidshallowbreathingindexasapredictoroffailureof noninvasiveventilationforpatientswithacuterespiratoryfailure.Respir.Care 57,1548–1554,http://dx.doi.org/10.4187/respcare.01597.
Brandão,D.C.,Lage,S.M.,Britto,R.R.,Parreira,V.F.,deOliveira,W.A.,Martins,S.M., Aliverti,A.,deAndradeCarvalho,L.,doNascimentoJunior,J.F.,Alcoforado,L., Remígio,I.,deAndrade,A.D.,2012.Chestwallregionalvolumeinheartfailure patientsduringinspiratoryloadedbreathing.Respir.Physiol.Neurobiol.180, 269–274,http://dx.doi.org/10.1016/j.resp.2011.12.002.
Britto,R.R.,Zampa,C.C.,deOliveira,T.A.,Prado,L.F.,Parreira,V.F.,2009.Effectsof theagingprocessonrespiratoryfunction.Gerontology55,505–510,http://dx. doi.org/10.1159/000235853.
Cohn,D.,Benditt,J.O.,Eveloff,S.,McCool,F.D.,1997.Diaphragmthickeningduring inspiration.J.Appl.Physiol.83,291–296.
DeAndrade,A.D.,Silva,T.N.S.,Vasconcelos,H.,Marcelino,M.,Rodrigues-Machado, M.G.,Filho,V.C.G.,Moraes,N.H.,Marinho,P.E.M.,Amorim,C.F.,2005. Inspiratorymuscularactivationduringthresholdtherapyinelderlyhealthy andpatientswithCOPD.J.Electromyogr.Kinesiol.15,631–639,http://dx.doi. org/10.1016/j.jelekin.2005.06.002.
Downey,A.E.,Chenoweth,L.M.,Townsend,D.K.,Ranum,J.D.,Ferguson,C.S.,Harms, C.A.,2007.Effectsofinspiratorymuscletrainingonexerciseresponsesin normoxiaandhypoxia.Respir.Physiol.Neurobiol.156,137–146,http://dx.doi. org/10.1016/j.resp.2006.08.006.
Enright,S.J.,Unnithan,V.B.,2011.Effectofinspiratorymuscletrainingintensities onpulmonaryfunctionandworkcapacityinpeoplewhoarehealthy:a randomizedcontrolledtrial.Phys.Ther.91,894–905,http://dx.doi.org/10. 2522/ptj.20090413.
Evans,J.A.,Whitelaw,W.A.,2009.Theassessmentofmaximalrespiratorymouth pressuresinadults.Respir.Care54,1348–1359.
Gosselink,R.,DeVos,J.,VanDenHeuvel,S.P.,Segers,J.,Decramer,M.,Kwakkel,G., 2011.ImpactofinspiratorymuscletraininginpatientswithCOPD:whatisthe evidence?Eur.Respir.J.37,416–425,http://dx.doi.org/10.1183/09031936. 00031810.
Hostettler,S.,Illi,S.K.,Mohler,E.,Aliverti,A.,Spengler,C.M.,2011.Chestwall volumechangesduringinspiratoryloadedbreathing.Respir.Physiol. Neurobiol.175,130–139,http://dx.doi.org/10.1016/j.resp.2010.10.001. Illi,S.K.,Hostettler,S.,Aliverti,A.,Spengler,C.M.,2013.Compartmentalchestwall
volumechangesduringvolitionalhyperpnoeawithconstanttidalvolumein healthyindividuals.Respir.Physiol.Neurobiol.185,410–415,http://dx.doi. org/10.1016/j.resp.2012.08.018.
Illi,S.K.,Hostettler,S.,Mohler,E.,Aliverti,A.,Spengler,C.M.,2011.Compartmental chestwallvolumechangesduringvolitionalnormocapnichyperpnoea.Respir. Physiol.Neurobiol.177,294–300,http://dx.doi.org/10.1016/j.resp.2011.05. 007.
Kenny,A.M.,Dawson,L.,Kleppinger,A.,Iannuzzi-Sucich,M.,Judge,J.O.,2003.
Prevalenceofsarcopeniaandpredictorsofskeletalmusclemassinnonobese womenwhoarelong-termusersofestrogen-replacementtherapy.J.Gerontol. ABiol.Sci.Med.Sci.58,M436–40.
Lalley,P.M.,2013.Theagingrespiratorysystem—pulmonarystructure,function andneuralcontrol.Respir.Physiol.Neurobiol.187,199–210,http://dx.doi.org/ 10.1016/j.resp.2013.03.012.
Neder,J.A.,Andreoni,S.,Lerario,M.C.,Nery,L.E.,1999.Referencevaluesforlung functiontests.II.Maximalrespiratorypressuresandvoluntaryventilation.Rev. Bras.Pesqui.Med.Biol.32,719–727.
Nobre,M.E.P.,Lopes,F.,Cordeiro,L.,Marinho,P.E.M.,Silva,T.N.S.,Amorim,C., Cahalin,L.P.,DornelasdeAndrade,A.,2007.Inspiratorymuscleendurance testing:pulmonaryventilationandelectromyographicanalysis.Respir. Physiol.Neurobiol.155,41–48,http://dx.doi.org/10.1016/j.resp.2006.04.005. Paisani,D.,de,M.,Lunardi,A.C.,daSilva,C.C.B.M.,Porras,D.C.,Tanaka,C.,Carvalho,
C.R.F.,2013.Volumeratherthanflowincentivespirometryiseffectivein improvingchestwallexpansionandabdominaldisplacementusing optoelectronicplethysmography.Respir.Care58,1360–1366,http://dx.doi. org/10.4187/respcare.02037.
Parreira,V.F.,Vieira,D.S.R.,Myrrh,M.A.C.,Pessoa,I.M.B.S.,Lage,S.M.,Britto,R.R., 2012.Optoelectronicplethysmography:areviewoftheliterature.Braz.J.Phys. Ther.16,439–453.
Pereira,C.,Sato,T.,Rodrigues,S.,2007.Newreferencevaluesforforcedspirometry inwhiteadultsinBrazil.J.Bras.Pneumol.33,397–406.
Phillips,D.B.,Stickland,M.K.,Petersen,S.R.,2015.Ventilatoryresponsesto prolongedexercisewithheavyloadcarriage.Eur.J.Appl.Physiol.,http://dx. doi.org/10.1007/s00421-015-3240-7.
Plentz,R.D.M.,Sbruzzi,G.,Ribeiro,R.A.,Ferreira,J.B.,DalLago,P.,2012.Inspiratory muscletraininginpatientswithheartfailure:meta-analysisofrandomized trials.Arq.Bras.Cardiol.99,762–771.
Rossi,A.,Fantin,F.,DiFrancesco,V.,Guariento,S.,Giuliano,K.,Fontana,G., Micciolo,R.,Solerte,S.B.,Bosello,O.,Zamboni,M.,2008.Bodycompositionand pulmonaryfunctionintheelderly:a7-yearlongitudinalstudy.Int.J.Obes.32, 1423–1430,http://dx.doi.org/10.1038/ijo.2008.103.
Souza,A.C.,Magalhães,L.,de,C.,Teixeira-Salmela,L.F.,2006.Cross-cultural adaptationandanalysisofthepsychometricpropertiesintheBrazilianversion ofthehumanactivityprofile.Cad.SaudePublica22,2623–2636.
Souza,H.,Rocha,T.,Pessoa,M.,Rattes,C.,Brandão,D.,Fregonezi,G.,Campos,S., Aliverti,A.,Dornelas,A.,2014.Effectsofinspiratorymuscletraininginelderly womenonrespiratorymusclestrength,diaphragmthicknessandmobility.J. Gerontol.ABiol.Sci.Med.Sci.69,1545–1553,http://dx.doi.org/10.1093/ gerona/glu182.
