DOI10.1007/s00198-013-2346-1
REVIEW
Theeffectofphysicalexerciseonbonedensityinmiddle-agedandoldermen:Asystematicreview
K.A.Bolam&J.G.Z.vanUffelen&D.R.Taaffe
Received:22November2012/Accepted:8March2013
#InternationalOsteoporosisFoundationandNationalOsteoporosisFoundation2013
AbstractAlthoughtrialshaveshownthatexercisehaspos-itiveeffectsonbonemineraldensity(BMD),themajorityofexercisetrialshavebeenconductedinolderwomen.Theaimofthisstudywastosystematicallyreviewtrialsexaminingtheeffectofweight-bearingandresistance-basedexercisemodal-itiesontheBMDofhipandlumbarspineofmiddle-agedandoldermen.EightelectronicdatabasesweresearchedinAugust2012.Randomisedcontrolledorcontrolledtrialsthatassessedtheeffectofweight-bearingandresistance-basedexercisein-terventionsonBMDmeasuredbydual-energyx-rayabsorp-tiometry,andreportedeffectsinmiddle-agedandoldermenwereincluded.Eighttrialsdetailedinninepaperswerein-cluded.Theinterventionsincludedwalking(n=2),resistancetraining(n=3),walking+resistancetraining(n=1),resistancetraining+impact-loadingactivities(n=1)andresistancetrain-ing+TaiChi(n=1).Fiveoftheeighttrialsachievedascoreoflessthan50%onthemodifiedDelphiqualityratingscale.Further,therewasheterogeneityinthetype,intensity,frequen-cyanddurationoftheexerciseregimens.Effectsofexercisevariedgreatlyamongstudies,withsixinterventionshavingapositiveeffectonBMDandtwointerventionshavingnosignificanteffect.Itappearsthatresistancetrainingaloneor
K.A.Bolam(*):J.G.Z.vanUffelen:D.R.TaaffeSchoolofHumanMovementStudies,
TheUniversityofQueensland,Brisbane,QLD,Australiae-mail:k.bolam@uq.edu.au
J.G.Z.vanUffelen
InstituteofSport,ExerciseandActiveLiving,VictoriaUniversity,Melbourne,VIC,Australia
D.R.Taaffe
SchoolofEnvironmentalandLifeSciences,
TheUniversityofNewcastle,Ourimbah,NSW,AustraliaD.R.Taaffe
EdithCowanUniversityHealthandWellnessInstitute,EdithCowanUniversity,Joondalup,WA,Australia
incombinationwithimpact-loadingactivitiesaremostosteo-genicforthispopulation,whereasthewalkingtrialshadlimitedeffectonBMD.Therefore,regularresistancetrainingandimpact-loadingactivitiesshouldbeconsideredasastrat-egytopreventosteoporosisinmiddle-agedandoldermen.Highqualityrandomisedcontrolledtrialsareneededtoestab-lishtheoptimalexerciseprescription.
KeywordsAgeing.Bone.Exercise.Men.Osteoporosis.Systematicreview
Introduction
Withtheageingofthepopulation,developingsafeandeffec-tivestrategiestopreventosteoporosisandconsequentfrac-turesisofgreatimportance.Themechanismsthatunderpinbonemineraldensity(BMD)declinefollowingpeakbonemassaremultifacetedandcomplexinnature.Althoughchangesinsexhormones,nutritionandbone-loadingareresponsibleforbonelossacrossthelifespaninmalesandfemales,importantgender-specificdifferencesexist[1,2].Thedeclineinbonemassinmenuptotheageof50andinpremenopausalwomenisapproximately0.3to1.1%peryear[3],withanacceleratedrateofbonelossinwomenfor4to8yearsfollowingmenopause[4]duetooestrogenwithdrawal.Duringthisperiod,womenwillloseapproximately15%inBMDoronestandarddeviation,leadingtoa1.5-to3-foldincreaseinfracturerisk[5,6].Incontrast,thedeclineinbonemassformenismoregradualwithanage-relatedlossof~0.7%peryearaftertheageof50[3].Nonetheless,approxi-matelyonethirdofallosteoporoticfracturesareaccountedforbymiddle-agedandoldermen[7],andsounderstandingtherolepreventativestrategies,(forexampleexercise)mayhaveinattenuatingthebonelossexperiencedbymeninthisagegroupisofgreatimportance.
Regularphysicalexercisehasbeenrecommendedasalow-costandsafenon-pharmacologicalstrategytocounterthelossofbonemassthataccompaniesageing.Theprinci-plesofeffectiveboneloadingaresomewhatuniquecom-paredtotheexerciseresponseofotherbodysystemssuchasthemuscularorcardiovascularsystems.Ithaslongbeenestablishedthattoimprovebonedensity,bonetissuemustbesubjectedtomechanicalloadingabovethatexperiencedindailyactivities[8].Mechanicalloadingshouldbedynam-ic,novelandinvolvehighstrainmagnitudesandratesresultinginsubstantialoverload[8,9].
Todate,theeffectsofexerciseontheskeletonhavebeenexaminedpredominantlyinpre-andpost-menopausalwom-en[10–17]duetothehigherratesofosteoporosisinwomenthaninmen.Reviewsoftheseexercisetrialsindicatethat,inwomen,thecombinationofhigh-impactloadingexercisesandmoderatetohighintensityresistancetrainingisthemostbeneficialtopreventage-relatedboneloss[13–15,17,18].However,olderwomennotonlyhavedifferentratesofbonelosscomparedtooldermen,butduringmenopausetheskeleton'sresponsetoloadingisdampened[19]duetothereducedsensitivityofbonecells[20].Consequently,theresponseofbonetoexerciseisdissimilarbetweenmiddle-agedmenandwomenduringthefirstfewyearsfollowingtheonsetofmenopause[21].
Astheburdenofosteoporosisinmenisbecomingin-creasinglyrecognised[22],asmallbutgrowingnumberofexerciseinterventionshavebeentrialledinmen.RecentreviewsoftheeffectofexerciseontheBMDofmaleandfemaleadults[23]andolderadults[18]havefocusedontheeffectsonBMDinwomen.Toourknowledge,onlyonereviewbyKelleyandcolleagues[24]hasexclusivelyfo-cusedontheeffectofexerciseinterventionsonBMDinmen.Oftheeightinterventionsincludedinthereview[24],onlytwouseddualx-rayabsorptiometry(DXA)tomeasureBMDofmiddle-agedoroldermaleparticipants,whiletheremainingstudiesrecruitedexclusivelyyoungerparticipantsorusedothermethodstoassessBMD.Theauthors[24]concludedthatexercisemayhelpimproveormaintainbonedensity,butthatmoretrialswererequiredtoconfirmthebenefitsinmen.However,thereviewbyKelleyetal.[24]waspublishedoveradecadeagoandthereforeanupdatedreviewoftheeffectsofexerciseonthebonehealthofmiddle-agedandoldermeniswarranted.
Moreover,thereissomediscrepancybetweenthecon-clusionsofboneandexercisereviews[17,18,23]andrecentinternationalpractiseguidelinesforosteoporosisinmen[22].Thesenewguidelinesrecommendactivitiessuchaswalkingasapreventativestrategyforosteoporosisde-spiteanapparentlackofsupportingevidencefromrandomisedcontrolledtrials.Whilstwalkingisbeneficialforanarrayofhealthoutcomes,itsprescriptionasastand-aloneosteoporosispreventionstrategyisinconsistentwith
OsteoporosInt
thecurrentAmericanCollegeofSportsMedicine(ACSM)positionstandonphysicalactivityforbonehealth[25].Withanageingpopulationandthusanincreasingpreva-lenceofosteoporosisinmen,thereisagrowingurgencyforhealthprofessionalstodevelopevidence-basedexerciseguidelinesformen.Therefore,theaimofthissystematicreviewwastoexamineboththefindingsandthestudyqualityofexercisetrialsexaminingtheeffectofweight-bearingandresistance-basedmodalitiesonBMDofthehipandlumbarspineinmiddle-agedandoldermen.
MethodsLiteraturesearch
WeconductedsearchesinthedatabasesPubMed,EMBASE(viaEMBASE.com),CENTRAL(CochraneCentralRegisterofControlledTrials),PEDroandSPORTDiscusinAugust2012.Searchtermsincludedcombinationsofthesaurusterms(MeSHinPubMed,CENTRAL,EMtreeinEMBASE)andfreetextterms.Freetermsforexercise(‘resistance*training’,‘‘strengthening‘jump*’,‘bounding’,‘exercise’,‘skipping’,‘weight*lifting’,‘hopping’’,,‘‘weight*bearingimpact*loading’’,‘high*impactleap*’,‘weight*training’,‘running’’,,‘‘stair*climbingresistance’,‘strength’,‘jogging’)were’,‘walk*usedin’,,AND-combinationwiththesearchtermsexpressingthetargetpopulation(‘men’,‘adults’,‘patients’,‘participants’,‘subjects’,‘people’,middle*aged’,‘aged’,‘aged,80andover’)andsearchtermsrepresentingbonedensity(e.g.‘bone*density’,‘‘bone*strengthmetabolic*bone*disease’,‘bone*mass’).In’,PubMed,‘bone*mineralsearch’results,‘bone*tissuewerelim-’,itedbysearchtermsindicatingspecificstudydesigns(e.g.‘trial’,‘random’,‘intervention’,‘pilot*study’).Thecompletelistofsearchtermsisavailableonrequest.Inclusioncriteria
Theinclusioncriteriawere:(1)design:randomisedcon-trolledtrials(RCT)orcontrolledtrials(CT);(2)population:middle-agedoroldermen(45yearsandolder).Studiesinmiddle-agedandoldermenandstudiesincludingmenandwomeninwhichresultsformenandwomenwerereportedseparatelywereeligibleforinclusion;(3)intervention:anyexerciseprotocolinvolvingresistancetrainingonly,impactloadingexerciseonly,weight-bearingaerobicexerciseonlyoracombinationofthesetypesofexercise;and(4)out-come:BMD(g/cm2)ofthelumbarspine,Ward'striangle,trochanter,proximalfemur,femoralneckortotalhipmea-suredbyDXA.Onlyfull-textarticleswereincluded,andnorestrictionswereplacedonthelanguageofthearticle.Titlesandabstractsofarticlesidentifiedthroughthesearchpro-cesswerereviewedfirstbyK.A.Btoexcludearticlesoutof
OsteoporosInt
scope.Subsequently,K.A.B.,J.G.Z.v.U.andD.R.T.inde-pendentlyreviewedthefulltextsofallpotentiallyrelevantarticlesforeligibility.Disagreementswerediscussedandresolved.Articlesthatmettheinclusioncriteriawerealsoexaminedtoensurethatthesamesubjectswerenotincludedinmorethanonearticlebasedondatafromthesamestudy.Referencelistsofeligiblearticlesweremanuallycheckedforadditionalreferences.
Qualityassessmentanddataextraction
Dataonthestudypopulation,exerciseprogrammesandoutcomemeasureswereextractedindependentlybytwoauthors(K.A.B.andD.R.T.).Onthebasisofprogrammedescriptionsintheindividualstudies,programmeswerequalifiedbyanexercisephysiologistasweight-bearingaer-obic,strengthtraining,impact-loadingexerciseoracombi-nationthereof.Methodologicalqualityoftheincludedreviewswasindependentlydeterminedbytwoofthethreeauthors(K.A.B.andD.R.T.orJ.G.Z.v.U.)usingtheDelphilistdevelopedbyVerhagenetal.[26].Thislistconsistsofninequalitycriteriaassessingdifferentmethodologicalas-pects.Twooftheninecriteria(i.e.blindingofthetrainersandblindingoftheparticipants)werenotappropriateforthetypeofinterventionswewerereviewing,andtheseitemswereexcluded.Thus,qualityofincludedstudieswasexam-inedusingasevenitemqualityratinglist[26,27].1.Wasthemethodofrandomisationperformed?2.Wasthetreatmentallocationconcealed?
3a.Werethegroupssimilaratbaselineregardingthemost
prognosticindicators?
3b.Ifgroupsweren'tsimilaratbaseline,wasthisadjusted
forintheanalyses?
4.Weretheeligibilitycriteriaspecified?5.Wastheoutcomeassessorblinded?
6.Werepointestimatesandmeasuresofvariability
presentedforBMD?
7.Didtheanalysisincludeanintention-to-treatanalysis
(ITT)(definedasallofparticipantsrandomisedwereincludedinanalysis)?Allcriteriawereequallyratedusinga‘yes’(1),‘no’(0),or‘unclear’(0)answerformat,andaqualityscorewasgeneratedasapercentageofthemaximumscoreforeachincludedstudy.
Results
Thesystematicsearchresultedin3,106records;detailsofthesearchprocessareshowninFig.1.Abstractsof3,106articleswereinitiallyreviewed.Afterremovingarticlesoutofscope,thefulltextof42articleswasindependentlycheckedfor
Records identified through database searching = 4859Duplicatesremoved by EndNote = 1753Records excluded = 3064of which 135duplicates were Abstractsscreened= 3106manuallyremoved Full text papers assessed for Full text papers excluded with eligibility = 42reasons = 33Men and women’s data not Papers identified as eligible = 9analysed separately Outcome not measured by DXA Participants were too youngAdditional papers identified Didnot meet inclusion criteria though reference lists of selected for interventionpapers = 0No control groupDidnot meet inclusion criteria for control group 9papers included describing 8Full text not available interventionsFig.1Searchprocessflowchart
eligibility.Thirty-threearticleswereexcluded.Checkingthereferencelistsofeligiblearticlesdidnotresultinadditionalarticles.Ninearticlesfromeightstudiesmettheinclusioncriteria[28–36].Oneinterventionwasdescribedintwoarti-cles,butwithdifferentdurationsofintervention[30,31].Botharticlesareincludedandareconsideredastheoneintervention.Qualityassessment
TheresultsofthemethodologicalqualityassessmentarepresentedinTable1.Qualityscoresrangedfrom29to100%withthreeoftheeightstudiesscoringover50%.AlthoughsixoftheincludedstudieswereRCTs,randomisationwasnotconcealedintwooftheseRCTs.Methodologicalaspectsthatwerenotscoredpositivelyinmostoftheeightincludedstudieswerereportingofpointestimates(includedinonestudy[30,31]),blindingoftheoutcomeassessor(includedinthreestudies[28,30,31,33])andconductinganITTanalysis(includedfourstudies[30–33,36]).Allofthestudiesscoredwellforgroupsimilarityatbaseline[28–36]andfiveoftheeightspecifiedeligibilitycriteria[28–32,35].
Studypopulationandexerciseprogrammes
CharacteristicsofthestudyparticipantsandexerciseprogrammesareshowninTable2.Participantsinthestudiesweremiddle-agedandoldermenpredominantlyfromnon-clinicalpopulations,butonestudyincludedhearttransplantpatientsonglucocorticoidtreatment[36].Samplesizes
)e%%%%%%%%Iro0C(cS3309397844124257slavrestisniylenaconniaetndtieaftennr8oItc6otYNYNYYNN/4ro)EsSe(tarmsoeyritrtruieslesidabrteaanmirdioanPdvatnf8s5aoNNYNNNNN/1,)DSr(osnsoeitsasidaveeeddnmdiorlBcatua8d4oUUaYUaYUNY/3natsr?eahtiireetidrndcaeiyeftiigclneiapbihSgci8s3leNNYYNYYY/5puorygtinreaelimwtiesebpniyuletioslsiraGbrb8oaYYYYYYYY/i2ta8hrtasuvraofheodthesutleaaremuceoshratntfenoecmnmmoonidrttaofanietaanmsTrcoreoiottfblaUYYNUNa6YY/amn1la4imirltoasfnennotiiotniilitadoandpsioa,mistigrodneddipnaniaapRgatda8nbin1YYYNYNYY/6tosaedsunnqao.eitrgebnarl3)rib1bu).eta09b)tsfed00)0gtt).aug03)1nn)2rqn211940iraeei6(r9.(090)2ot()sereal9la.2rl(104.7csrcrff1a(29(lei.9a0net(te,0srpydtl..ufeall1tatati.l,a(e2e(ppluaan,ta.Udnettl,.alburteea,ea,edlpaarat,Qenlj,totlnotfoYetnara,ouasdefeo/ihkjerrtsklet1,rtr,iauuka,lntoenNytoikneleiairuubie,lhBHKuahsm.KMPRyWWomolbtpeauyua..a.....uaTaAQS12345678NYabOsteoporosInt
rangedfrom11to147men,withparticipantsaged50to79years.Thedurationoftheprogrammesrangedfrom3monthsto4years(mean13months)withDXAassess-mentsatthestartandaftercompletionoftheexerciseprogrammes.Inthehearttransplantationstudy,Braithandcolleagues[36]alsomeasuredtheBMDofparticipants2monthspriortocommencingtheexerciseinterventiontoassesstheimpactofglucocorticoidtherapyfollowingtrans-plantation.ChangesinBMDovertheinitial2monthspriortoexercisearealsoreportedinTable2.Oftheeightexerciseprogrammes,twoincludedwalkingonly,threeincludedresistancetrainingonly,oneincludedwalkingandresistancetraining,oneincludedresistancetrainingandimpact-loadingactivitiesandoneincludedresistancetrainingandTaiChi.Themajorityoftheprogrammesprescribedthreeexercisesessionsaweek(rangingfrom2–5eachweek).Theprescribedintensitiesoftheinterventionsvariedgreatly.Withinthetrialsthatincludedresistanceexercises,intensityinallbutoneoftheinterventionsusedindividualisedinten-sities;percentageof1-RM[30,31],whereRMorrepetitionmaximumisthemaximumamountthatcanbemovedorliftedonetimeonly,8-RM[29]or5–15-RM[35].TheexceptionwasthestudybyWooetal.[28],whodidnotreportintensitybutinsteadtheparticipantsweresup-pliedwithamediumstrengthelasticband(Theraband)forresistance.Thetwotrialsinvolvingaerobicexerciserequiredtheparticipantstowalkatabriskpacecorre-spondingto40–60%oftheirmaximaloxygenuptake[34]ortheirlactatethreshold[33].ThejumpingprogrammeinthetrialbyKukuljanandcolleges[30,31]requiredtheparticipantstoperformimpact-loadingactivitieswithgroundreactionforcesrangingfrom1.5to9.7timesbodyweight.
Fouroftheeighttrialsweresupervised,andinthema-jorityofcasesthiswasbyexercisespecialists/exercisephysiologists.Inadditiontoanexercisespecialist,inthetrialbyMenkesandcolleagues[35],registerednursesandphysicaltherapistswerethesupervisors.Threeofthestudiesdidnotreportifthesessionsweresupervised[28,32,33],andonewasunsupervised[34].Machineandfreeweightswereusedinalloftheresistancetrainingprotocolswiththeexceptionoftheonetrialthatusedelasticbands[28].Noequipmentwasusedbytheparticipantsinthewalkingin-terventions,whiletheimpact-loadinginterventionusedbox-esandbenches[30,31].Whilealloftheeightstudiesincludedcontrolgroups,onlyfourdescribedtheinstructionsgiventotheseparticipants,andthesewerepoorlydetailed[28,29,34,36].Braithetal.[36]comparedtheirinterven-tionwithapost-operativewalkingprogramme;Huuskonenetal.[34]advisedthecontrolgroupparticipantstomaketheirpersonalchoicewhethertoengageinphysicalactivityornot;Whitefordandcolleagues[29]providedtheircontrolgroupwitheducationandadvisedthemtowalkfor30min
WithingroupschangeOsteoporosInt
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S↑0.6%N−0.8%othip↑0.2%xS↑2.0%aN↑3.8%aon(numericaldatanotreported)S↔N↔xip−1.2%onip−3.3%xS−0.1%N↑2.8%aWhcLFTELFCspautoadrdetglraoncpeieerewgerntmto↔↔eaunBhcNSLNFtnaDrMewbtB’mnetudienDlpt(um)go2onpcito=sroettDxE,n,oniswnoetdxgleel,lnlusoospp,lkirternttht:angacuuicrDlrt:roit,g,IRuceds:w,sdens&neelot,ieSnoersoipastesciCerfcy,stseurrcs,sdeneedexescnhw,pdaeu:naaCogrselg,qDtdse:ne)krlelrSnnefeiBcu:ac)B,mt:y,thUbsnopFtiacsa(rpLit:ni,tsee(cdtmounnepcsiuespbesdiiqoetA,iteisntnai,ecuilbfirlc,ade,r:nseserveutoixsbegorpiceydnIsreebxemierlttnn,vxypme,s,sieresosdruynnhktipeitToeddooonw/scneerpbdiisldbsssoireRcerernnpmyarxv&us3euteer:1poaeeeuttxesttpphewxx-4dtssET:neuisST:Uoeeis:3LD:IF,dDnaS)))s±s4dtr.enneaage47gepay4±a-mi(cn=9e.lride8taeregn9ddl1ao5(i=Pmna(rCMonyndgiustTSedCklyi)rmdtendt]uuno5noan3itCnksw,[.los)ripe)lciamui3vA,9(aetey+ordesr9e2d(ege1rssk(ieiedcnulhn.llyobdhrteauteoclTatuxannMtAiiSAE.eS4ULFEHCHELF%%4.11%.s2'd5.pr1iHWaTrlliiNNegseilcssrt,peohngtexgregiwel5,tneo,i1s)idwdnoli,nelttpdeeaoeucsrbeirprpufstd1hcedadtsrnlaBlerUadoa,lccsrgiteuel;soysnc,tipynishgsseh(rp’snceelrea5,lt1eosrnm,pssrrti,ee,sunddsrtelddepdlesodesutsMdnoecgnitilhnetetrcso2Rtdreei5orvksasirrorehlhkuemoopehsB1pesitttatrpL-esscnwexc,/dih0epre,nosvt6rersoti:MriiwlatgRRoea%nkiimyie–ttadtooTs5nrc5‘sia5noResrn3dnit4nn&:e9:rc::4pet::p:ttnB:5:::1gxSnDpustDta:nlDputnteeISSAoCT:IFISSAoCT:L)))EEn0.nSSe2±em)2±700ddm..er766er21ge–6(±7±ad3(0ge-l61ad-l1100eo(11eo.l=9=.dd1=)ldn2=n0dd7.3x5n5(o5(iECMa=xo2dninECMa=nTCTRC]]3233[,[,).T.4S)4,0.d0r2A99a(,1ll.n(ilea.laacaPtn.eaRytAreS5F.6Uard's−0.2%r−0.1%onS,FN↔(numericaldatanotreported)ard's−1.6%r−1.6%ithingroupsangeTS−0.1%N−0.3%r↑2.2%aothip↑0.8%aonS−0.1%N−0.6%r↑2.2%aothip↑0.8%aTS↑1.3%othip−1.2%aiChiS↑1.4%othip−0.5%OsteoporosInt
WhcWTCLoltacei)lrdsbeetparunmoouupr(negn↔,rettaoeeeNlunwgnFcaltta,aaehScdBcLrebmuntuoporDylr,e,nlnloowrtoueirocsettln:an,sdiD:rspnhse2cIRuocd:eca,riss&pbemeSnnssoois,igicy,sCpslcercs,earleneecnexesciixdreu:ntmena,qDatnew,ollldarrSdnefobrurmaoc:y,etttkfrgpFiasceseni,n:tapplounetbpe,stiqoteinArusrlsnti,e,a5ee,a:npnn1rvertpoiprpunoiuieydIssm,tgMitt,,oseRnsvnnedhkel5tiensoprotbnwst/r1eiieeitxaosso-fsctrpceirnceeurMemy1a:5rxv&us:dkceersbaw4dR1R5xetpabo:3flET:tneuD&:o:tnisSIFSI,))DEES))SSs±s00tr..nea1age62pay1±1±i(21cn.=2.ieta=1regn9anx6(o5(Pma(rECyndgiustSedy)rdtenuunoitCnos)rlcia(aetey2d(relyobdhutTatuSAWTRLFTTCLFTTRLTTLTc%ich1C%%↔T.i3.R%1↔3ppTa%0.i0↔ihv8.n0hv9p.iStotn0hoStLNFTrToCSLToCLTo61511====TnoTnoRCRCd,entroonkispsitoextiriihhnteelgwmraoacwfti,en,emurpowonrdeinith,twofs)eco,poep,enTeudlenhsttysoiRrrsliifdhrubscdau8iax(gorwadretldns,oslnd3/slfinapppistoesdes)aeoicdnerishpecssiniahohbei,enncb3yevvomb,dCcniitihoir,itlcsr→hpirt0cgscp3iotinTaalan,eunsestitsaemescopri,kactdseluatitiecxastpelaedunpeht)eriaruwr,bqagiddd,sreen5MreowsaseedirseT0nhtetpfltrsiawp1Rxep,3eCrsgtnotsinRrrthceooroicsuh,s8aihos(,tisstktpdcihtppoppr,,seene→deTRier,eeerxnnr/rrreooeowscsegstkeTasm(/iittiivnttxteoimstnnneow/uy3Mniifrvxeitt2idooooTecrt:Rmila%adfxmsydennnnRlua,2a50u1PaTi:tle2a::fdlnr1dR16q7Rer::dR::Dp8:3:::nnmp1dmoiutnpduortiacpSSAoCT:HD&t:Dputto6arh:3&p:teIFSnISSACT:AD:rIFSnIddnnaa)d))d4en00en7)0ge..ge–.a646a-m-m5360±e3±7±elr7700lr(de4..de37ddl1=4=4dd0=.8l9iiMo=x6n6(o(nECMo=T6(nRTTCCRR]9,..2lJ[a,)td0e]r18o0,g.2fJ[ne2aot(i,)ilh.o7Kla0WarttsWo0g2n.eu.(o7A8HOsteoporosInt
xraTm,2kcsep%VOnu2,lo%.oar0trgo5−ne.gnm0pigiiehnsfn↑htiaotsWheNCSLTocrgFo,repni→psrs,apgbunoimrnugilanrSteLeee,wgnc)tn2eaaBhtmcsci/sge(ryTtiRsn,emdrulebmariemxnuainmmtseuonnpooibotirtDeDpMerB,MthRgi,ekeweywd,onlkbooirwttW,:ansBD:ron,IRucog:i,tns&dniieSnotsoediaiCpcy,sseolrcs,r-eneemtxescrsceu:naopaf’ep,qDtd%neRmrSn14diefe82eb,mtl:y,ttihiroLIdpFiatcshiretti,:unntCny,rntwserqoeodootepcopiteiAitnlbeni,,ayenreer:nddTatssioreevputoee,titydnIsrr%gcrCwgrentti,ne,oanensvooxrpp3.plhisopeee6YaeuBceiicteorprrt7t:orLosirnneeooTi‘gy,ncrxv&usnnRh::C:edeeres::nso↔xttpoiET:neuDputitcb,isSSSATaCrreeesxpaeper,DxucS))EBnpiu)s±s0)7,lU↑ortr4.nea3.2a,ie,gage2rpltcpay=±0±3rii(i7cnh20..dohorieflttaelanregC8=8lntani6n6oooocPma(o(rit(rTaCttncpnoaiacehshrttTdpepCnTonuuu,iolroyn,loeegrdgarlsgiusigganrtFnbeetSedaesidRirmwcetrotelGlsreo,'fbxyredetkree)rnaccndtotnnenucpWaieesuusrrsod'eeonliCenfffftserdiinigds)myWadDorlttcianM(aeoxntdor,aaBeynletcc2rd(iiraanffermaiitelyonnbdhutTihaggetuCxaciirTaoSARmrSSGtabc3daysperweek,andWooetal.[28]reportedthatthecontrolgroupwasnotprescribedanyexercise.Reportedfindings
TheeffectsoftheinterventionsonBMDareshowninTable2.BMDofthelumbarspinewasreportedinsevenoftheeightstudies[28,29,31,32,34–36].Inaddition,femoralneckBMDwasreportedinfive[29,31,32,35,36],totalhipBMDinthree[28,29,31],trochantericBMDinthree[29,31,32],bothWard'striangle[32]andproximalfemurBMDinone[34],whilePaillardandcolleagues[33]reportedonlythattheymeasuredhipBMD.
ThegreatestbetweengroupchangeinBMDwasinthetrialbyBraithetal.[36]amonghearttransplantpatients.Theonlystudytoincludehigh-impactloadingexerciseorhigh-velocitypowerresistancetrainingintheirtrialwasKukuljanetal.[31].Althoughthereweresignificantin-creasesinBMDinmostoftheresistancetrainingprogrammes,thestudybyKukuljanetal.wastheonlytrialtoreportasignificantdifferenceinBMD(femoralneck)betweentheexerciseandcontrolgroupfollowingtheinter-ventionperiod.BoththeexerciseandcontrolgrouplostBMDinthetrialsbyPaillardetal.[33],Ryanetal.[32]andWhitefordetal.[29]withtheexceptionoftheincreaseinfemoralneckBMDoftheexercisinggroupinthestudybyRyanetal.[32].Importantly,althoughnotstatisticallysignificant,theexercisegroupsalllostlessBMDthanthecontrolgroups,inallbutoneofthestudies[28].Conversely,inthetrialbyWooetal.[28],totalhipBMDofthoseintheelasticbandresistancegroupdeclinedmorethanindividualsinthecontrolgroup,althoughlumbarspineBMDofthecontrolandexercisegroupsincreased.Betweengroupdif-ferencesfortwoofthestudies[34,35]couldnotbecalcu-latedbecausenumericaldatawerenotreportedinthesepapers.
Dropout,attendanceandadverseevents
Fouroftheeightstudiesreportednodropoutsfromthecontrolorexercisegroups[32,33,35,36].Ofthetrialsthatdidreportdropout,theaverageratewas3.3%[28,29,31,34].Forthefourstudies[28–31,35]whoreporteddropoutbygroup,theoveralldropoutrateswere6.8and2.1%fortheexerciseandcontrolgroups,respectively.Reasonfordropoutincludedpersonalreasons[29,34],deathofpar-ticipants[34],illness[29,31]orworkandpersonalcom-mitments[29,31].Onlyfouroftheeightstudiesreportedattendancerates[28–31,35].Sixoftheeightstudiesdidnotincludeorreportanyadverseevents[28,32–36].Inthetwostudiesthatdid,Kukuljanandcolleagues[30,31]notedthatalthoughtherewerenoseriousoradverseeventsassociatedwiththeirexerciseregimen(exerciseonlyandtheexercise
andmilkgroups),anumberofmedicalcomplaintsoccurred.Theseincludedexacerbationoflongstandinggoutofthefoot(n=1),aggravatedkneeorhippain(n=2),lowerbackinjury(n=2)andaggravationofalongstandingshoulderinjury(n=2).Inaddition,threemensufferedaninguinalhernia.Allofthesemenwereabletocontinuewiththeprogrammeexceptforonemanwhoselongstandinglowerbackinjurycausedhimtowithdrawfromthetrial.Similarly,Whitefordetal.[29]notedthefollowingasreasonsgivenforwithdrawalfromtheirresistancetrainingprogramme:bypasssurgery(n=1),fractureofathoracicvertebra(n=1),hipreplacement(n=1),depression(n=1),hipproblems(n=1),chronicillness(n=1),moved(n=3),andpersonalreasons(n=7).Thesereasonswerenotreportedasadverseeventsassociatedwithorasaresultofparticipationintheresistancetrainingprogramme.FivemeninthetrialbyWhitefordetal.[29]withdrewfromthecontrolgroupduetodepression(n=1),movedawayfromthestudylocation(n=3)orforpersonalreasons(n=1).
Discussion
ThepurposeofthissystematicreviewwastoinvestigatetheeffectsofexerciseonhiporspineBMDinmiddle-agedandoldermen.Followingasearchoftheliterature,weidentifiedeightinterventionstudiesreportedinninejournalarticlesthatmettheinclusioncriteria.Theresultsfromthisreviewsupportthefindingsofsimilarreviewsinpre-andpost-menopausalwomenthatresistancetrainingandhigh-impactloadingactivitiesaremorelikelytoinducepositiveeffectsontheBMDofweight-bearingskeletalsitesthanwalking,whichisrelativelylow-impact.Nevertheless,theoptimalexerciseprescriptionformiddle-agedandoldermencannotbedeterminedfromtheresultsofthetrialsinthissystematicreviewduetovariationsinreportedBMDchangesandinthedesignoftheexerciseprogrammesandtherelativelypoormethodologicalqualityofanumberofthetrials.
Fiveoftheeighttrialsachievedaqualityratingscoreoflessthan50%onthemodifiedDelphiratingscale,andthereforecautionshouldbetakenwheninterpretingthere-sultsofthesestudiesduetotheirmethodologicalquality.Further,essentialinformationregardingmethodologicalqualitywasmissinginallincludedstudies,evenifthetrialitselfwasmethodologicallysound,andforallbutoneofthestudiesitwasnecessarytorequestfurtherinformationfromtheauthors.
OfthestudiesscoringhigherontheDelphiqualityratingscale,onlyKukuljanandcolleagues[30,31]scoredposi-tivelyonallmethodologicalitems.Theirtrialofresistancetrainingandhigh-impactloadingexercisewasalsotheonlytrialtofindsignificantbetweengroupeffectsatthefemoralneckfavouringtheexercisegroup.However,thissignificant
OsteoporosInt
differencebetweentheexerciseandcontrolgroupwasnotmirroredattheothermeasuredsites(lumbarspineortotalhip).Wooetal.[28]whoscoredthesecondhighestqualityratingreportedthattherewasnosignificantdifferencesbetweenthegroupsateitherthespineorhipsitealthoughonlyelasticbandswereusedastheresistance.Whitefordetal.[29]whoscored57%alsofoundnosignificantdiffer-encesinBMDbetweentheresistancetrainingandthecon-trolgroupsfollowingtheintervention.Allbutoneofthetrials[34]thatscoredlessthan50%reportedthatexercisehadapositiveeffectonBMD.Itisimportanttonotethattwoofthefourexerciseinterventionsthatreportedsignifi-cantwithingroupimprovementsinBMDallowedpartici-pantstochoosetheirgroupallocation.Thisnon-randomallocationmayhavebeenafurtherconfoundingfactorwith-inthesestudies,andresultsfromthesetwotrialsshouldbeinterpretedcautiously.Methodologicalaspectsthatshouldbeimprovedinfuturestudiesincludeprovidingpointesti-matesandmeasuresofvariability,blindingtheoutcomeassessor,concealingthetreatmentallocationandincludinganintention-to-treatanalysis.Itisimportanttodescribethiswellinfuturestudiessothatreaderscanappropriatelyappraisethequalityofthestudy.
Inadditiontomethodologicalqualityandreporting,theappropriatenessofthedesignofexercisetrialsmustbeconsideredwhendrawingconclusionsfromtheresults.Onlyfouroftheeightstudies[28–31,35]recordedandreportedattendanceratesoftheexercisegroups.Further,noneoftheeightstudiesreportedadherence,whichshouldnotbeconfusedwithattendance.Aparticipantcanattendanexercisesessionbutmightnotadheretotheexercisesasprescribedintermsofintensity,etc.Thefactthatthiswasnotconsistentlyreportedinthestudiesincludedinthisreviewisanimportantlimitation,whichcouldhaveresultedinanunderestimationofthetrueeffectofexerciseonBMDifattendanceandadherencerateswerelow.Consequently,westronglysuggestthatbothattendanceandadherenceratesbereportedinfutureinterventionstudiesexaminingtheeffectofexerciseonBMD.Inaddition,improvementsinbonedensityarerelativelymodestwithexerciseandoccuroveraprolongedperiodoftimeduetothelengthoftheremodelingcycle[25].Arecentreviewofexerciseregimens[18]showedthatexerciseregimensthatwereeffectiveinimprovingtheBMDofwomenwerecommonly12monthsorlongerinduration.Inthecurrentreview,onlyfouroftheeighttrials[28–31,34]were12monthsormoreinduration,andthereforetheresultsfromtrialsofshorterdurationmaynotaccuratelyreflecttheeffecttheseexercisemo-dalitiesmayhaveonBMDandmustbeinterpretedwithcaution.
Itisalsowellestablishedthattheintensityandnoveltyoftheloadaretwoofthemostimportanttrainingcharacteris-ticsthatinfluencetheeffectofexerciseonbone[37].Bone
OsteoporosInt
adaptstohabitualloadsandwithoutprogressingtheinten-sityofthemechanicalloadswithexercise,BMDwilllikelybemaintainedratherthanimproved[38].Despitethis,theintensityoftheexerciseprogrammeswasnotprogressedinthreeoftheeighttrials[28,33,34].Furthermore,thede-scriptionoftherateofprogressioninthefivestudiesthatdidincludeprogressionwasgenerallylackingindetails.Giventheimportanceofprogressionratherthancustomaryloadstoboneadaptation,researchersshouldaimtomakeintensityprogressionafocuswhendevelopingnewprotocols.Lessisknownabouttheoptimalfrequencyofexerciseforbonehealth.ArecentrandomisedcontrolledtrialinwomenbyBaileyandcolleagues[39]foundthatbriefboutsofimpactloadingexerciseweremorebeneficialwhencompleteddailythan4daysaweek.Whilebothofthesefrequenciesinducedincreasesinbonedensity,thoseinthegroupthatexercised2daysaweeksawnochangeintheirBMDandthecontrolgroup(noexercise)lostBMD.Fiveoftheeightprotocolsinthissystematicreviewrequiredparticipantstoexercise3dayseachweek.Therefore,itmaybethecasethatthefrequenciesofthesestudieswerenotoptimalforimprovingbonehealth.However,compliancetoexercisesessionsisanimportantpublichealthissueandinlightofthealreadylowlevelsofphysicalactivityparticipationamongstthepopula-tion,thechallengesassociatedwithaskingindividualstoexercisedailyaresignificant.Trialsthatfurtherourunder-standingofthedose–responserelationshipbetweenexerciseandbonearecertainlyrequired,particularlyinmen.
Incomparisontotheconsiderablylargernumberofex-ercisestudiesinmiddle-agedandolderwomen,theexistingcomparablestudiesinmenaregenerallyshorterindurationandhavefewerparticipants.Furthermore,agreaternumberofimpact-loadingexerciseinterventionshavebeenconductedinwomenthaninmen.Althoughtheresultsfromthetrialsexaminedinthissystematicreviewaresimilartotheexistingliteratureinpre-andpost-menopausalwomen[18,40,41],furthertrialsinmiddle-agedandoldermenarewarranted.
Onlyfiveoftheeightstudiesincludedtheparticipants'levelofexerciseparticipationintheirexclusioncriteria.Ryanetal.[32]andMenkesetal.[35]statedthatregularexerciseparticipationwaspartoftheirexclusioncriteria,butdidnotdefinethelevelsofparticipationthatwereacceptable.Wooetal.[28]statedthateligiblesubjectscouldnotbeparticipatinginTaiChiorresistancetrainingatthetimeofenteringthestudy,whichdoesnotcapturepastexercisepar-ticipation.Similarly,Whitefordetal.[29]specifiedthattheparticipantsshouldnotbeparticipatingin‘briskwalking’;however,likeWooetal.[28],theirinclusioncriteriadidnotcapturetheparticipants'levelofexerciseonentryintothestudynordiditexcluderegularwalkersexercisingatlesserintensities.Giventhatboneadaptsfavourablytonovelstimuli,failingtoassessandcontrolfortheparticipants'currentlevelofexerciseparticipationmayexplainthedifferentresponsestoaparticularexercisemodality.Further,onlythreeoftheeightinterventionsreportedthecalciumlevelsoftheparticipants[29–31,34],andfewerstillalsoreportedvitaminDstatus[30,31].GiventheimportantrolesofcalciumandvitaminDinbonemetabolism[42],itwouldbeprudenttosuggestthatdataoncalciumandvitaminDlevelsshouldbeincludedinfutureexercisetrials.TheexclusioncriteriadevelopedbyKukuljanetal.[31]werehighlyspecificandthusmoreclearlydescribedthestudypopulation.Futurestudiesshouldaimtoincludethislevelofdetailwhendesigningandreportingthedetailsoftrials.
Resultsofrecentmeta-analysesofdifferentexercisemo-dalities(aerobic,resistancetrainingandimpact-loading)onBMDinpost-menopausalwomen[43–45]supportthefind-ingsofthecurrentreviewinthattheeffectofexerciseonbonedensityofolderadultsappearstobemodalityandintensity-dependent.Specifically,itappearsthatresistancetrainingaloneorincombinationwithhigh-impactloadingactivitieshasthepotentialtoattenuateorreversethedeclineofBMDinmiddle-agedandoldermen.Includingresistancetrainingwouldalsoresultinimprovedphysicalfunction[46]andareductioninfallsriskduetoincreasedmusclestrength,thereforereducingtheriskforfracture[47].Whilemenshouldengageinregularwalkingduetoitspositiveeffectoncardiovascular,metabolicandpsychosocialhealth,theevidencefromthisreviewdoesnotsupporttheinclusionofwalkingaloneinexerciserecommendationsforthetargetedpreventionofosteoporosisinmiddle-agedandoldermen.Thisfindingissupportedbytheresultsofrecentreviewsthatindicatedthatwalkingalonewasnoteffectiveinincreasingthebonedensityofolderwomen[43,44].Nevertheless,atrialinperi-menopausalwomenindicatedthatbonedensityatthefemoralneckwasmaintainedfol-lowingaprogrammeofbriskwalkingandjogging[45].Further,briskwalkinghasbeenshowntohaveapositiveeffectonhipandspineBMDofpost-menopausalwomen[46,47].Althoughitwouldseemprudenttosuggestthatmenmayalsobenefitfrombriskwalking,futuretrialsareneededtoconfirmthisrecommendation.Consequently,re-centguidelinesforosteoporosisinmen[22]thathaverecommendedwalkingaloneasanosteoporosispreventionstrategyarenotconsistentwiththecurrentevidencebaseontheeffectofexerciseonBMDinmen.
Whilethereisaneedtodeterminetheoptimalexerciseprescriptionfor‘healthy’olderadults,clinicalpopulationsatriskforbonehealthissuesmayhavethemosttogainfromundertakinganappropriateosteogenicexerciseprogramme.Oneoftheeighttrialsinthisreviewwasconductedinhearttransplantpatients,receivingglucocorticoidtreatmentwhichhasadeleteriouseffectonbone[36].Theextenttowhichexerciseimprovedthebonedensityinthisclinicalgroupofpatientswasmostlikelyduetotherapidrateof
treatment-relatedbonelossimmediatelypriortotheexerciseintervention.Hence,thesenoteworthychangesinBMDareclearlynotreplicatedinhealthymenofacomparableage.Despitethis,thesepositiveeffectsareinaccordancewithresultsoftrialsinvolvingclinicalpopulationssimilarlyatriskofacceleratedratesofbonelosssuchasmenreceivingandrogensuppressiontherapyforprostatecancer[48]andwomenwithbreastcancer[49,50]andthuswouldsupporttheinclusionofexercisetrainingasanadjuvanttherapyforindividualsatriskofexperiencingtreatment-relatedboneloss.Despitethegreatpotentialthatexercisemayhaveinmanagingtreatment-relatedsideeffects,furthertrialsareneededtodeterminetheoptimalexerciseprescriptionforatriskclinicalpopulations.
Whileresistancetrainingaloneoracombinationofresis-tancetrainingandhigh-impactloadingactivitiesappeartobesafeandeffectiveinpreventingorreversingage-relatedbonelossinmiddle-agedandoldermen,theoptimalfrequency,sessionduration,intensityandexactexercisecombinationcannotbedeterminedfromtheresultsofthissystematicre-view.Incomparisontothelargenumberofexercisetrialsinwomen,osteoporosispreventionexercisetrialsinoldermenaresparse.Accordingly,theauthorsoftheACSMphysicalactivityandbonehealthpositionstand[25]havebasedtheirrecommendationsforolderadultspredominantlyfromthere-sultsoftrialsinwomen.Weproposethatbeforetheoptimalexerciseprescriptiontopreventosteoporosisinmiddle-agedandoldermencanbeprescribed,methodologicallyrobust,long-durationrandomisedcontrolledtrialsinthispopulationarerequired.Giventhatgender-specificfactorsinfluencebonemetabolism,wheretrialsrecruitmenandwomen,analysisshouldbeconductedbygender.Trialsinthisareaarelogisti-callychallengingduetoattrition,adherenceandthehighcostsofundertakingrelativelylong-durationinterventions,however,giventheageingofthepopulationandtheproportionofmenpotentiallyatriskforosteoporosis,effortstoaddresstheoste-ogenicexerciserequirementsformenareurgentlyrequired.Thissystematicreviewhasseverallimitationsthatareworthyofcomment.First,ouranalysisincludesonlydatafrompublishedstudiesandthepossibilityexistsofmissingrelevantunpublishedtrials.Second,therelativelysmallnum-berofparticipantsinanumberofthesestudiesmaylimittheabilitytodetectastatisticallysignificantdifferencebetweentheinterventionandcontrolgroups,andthisshouldbecon-sideredwheninterpretingtheresultsofthesestudies.Asaresult,itisstronglysuggestedthatstatisticalpowercalcula-tionsbeincludedinreportsoffutureinterventionstudies.Third,manyofthestudiesincludedinthisreviewdidnotreportthepost-interventionscores,orpost-interventiondatawerenotavailable.Inadditiontothis,duetotheheteroge-neousnatureoftheincludedexerciseprotocolsandthevari-ationinBMDmeasurementsites,ameta-analysiswasnotperformed.Lastly,itmustbenotedthatusingBMDas
OsteoporosInt
measuredbyDXAisafurtherlimitationofthisreviewduetoconcernsregardingtheinherentinaccuraciesofthismethodofmeasurementanditsinabilitytoprovideinformationre-gardingimportantdeterminantsofbonestrength(size,shapeandstructure)[51].Consequently,thereisgrowinginterestinusingquantitativecomputedtomography(QCT)toassessbonestrength,andresearchersshouldaimtousethismethodtoassesstheeffectsofexerciseinterventionsonwholebonestrengthwherepossible.Tothebestofourknowledge,onlyoneexercisetrialhasusedQCTtoassessbonestrengthinmiddle-agedandoldermen[31].Whilethereisapossibilitythatsomestudiesweremissedintheliteraturesearch,itismorelikelythatthesmallnumberoftrialsinthissystematicreviewreflectsthestrongfocusonpreventingosteoporosisinwomenratherthaninmen.Safetyaspects
Althoughresistancetrainingandimpact-loadingactivitiesap-peartobesafemethodsofexercisetraining,olderadultsshouldbecarefullyscreenedandsupervisedpriortoandduringexerciseparticipationtoensuresafetyandcorrecttechnique.Whereappropriate,cliniciansshouldreferpatientstoappro-priatehealthprofessionals,suchasexercisephysiologistsorphysiotherapists,trainedtoprescribeexerciseforindividualswithchronicdiseaseandassociatedco-morbidities.
Conclusion
Resultsfromthissystematicreviewindicatethatresistancetrainingaloneorincombinationwithimpact-loadingactiv-itiesissafeandmayassistinthepreventionofosteoporosisinmiddle-agedandoldermen.However,duetothevaria-tionamongstudiesaswellasinstudyquality,additionalhigh-qualityrandomisedcontrolledtrialsinthispopulationarerequiredinordertoestablishevidence-basedguidelinesfortheoptimalexerciseprescription.Nevertheless,forthoseindividualswillingandabletoperformphysicalexercise,regularresistancetrainingandimpact-loadingactivitiesshouldbeconsideredasaneffectivestrategytopreventosteoporosisinmiddle-agedandoldermen.
ConflictsofinterestNone.
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