23Selective impairments of restingstate networks in minimal hepatic encephalopathy.docx
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23Selective impairments of restingstate networks in minimal hepatic encephalopathy.docx
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23Selectiveimpairmentsofrestingstatenetworksinminimalhepaticencephalopathy
SelectiveImpairmentsofResting-StateNetworksinMinimalHepaticEncephalopathy
RongfengQi,
Affiliation:
DepartmentofMedicalImaging,JinlingHospital,ClinicalSchoolofMedicalCollege,NanjingUniversity,Nanjing,JiangsuProvince,China
X
LongJiangZhangequalcontributormail,
equalcontributorContributedequallytothisworkwith:
LongJiangZhang,GuangmingLu
*E-mail:
kevinzhanglongjiang@(LJZ);cjr.luguangming@(GL)
Affiliation:
DepartmentofMedicalImaging,JinlingHospital,ClinicalSchoolofMedicalCollege,NanjingUniversity,Nanjing,JiangsuProvince,China
X
QiangXu,
Affiliation:
KeyLaboratoryforNeuroInformationofMinistryofEducation,SchoolofLifeScienceandTechnology,UniversityofElectronicScienceandTechnologyofChina,SichuanProvince,China
X
JianhuiZhong,
Affiliation:
DepartmentofImagingSciences,UniversityofRochesterSchoolofMedicineandDentistry,Rochester,NewYork,UnitedStatesofAmerica
X
ShengyongWu,
Affiliation:
MedicalImagingInstituteofTianjin,Tianjin,China
X
ZhiqiangZhang,
Affiliation:
DepartmentofMedicalImaging,JinlingHospital,ClinicalSchoolofMedicalCollege,NanjingUniversity,Nanjing,JiangsuProvince,China
X
WeiLiao,
Affiliation:
KeyLaboratoryforNeuroInformationofMinistryofEducation,SchoolofLifeScienceandTechnology,UniversityofElectronicScienceandTechnologyofChina,SichuanProvince,China
X
LingNi,
Affiliation:
DepartmentofMedicalImaging,JinlingHospital,ClinicalSchoolofMedicalCollege,NanjingUniversity,Nanjing,JiangsuProvince,China
X
ZongjunZhang,
Affiliation:
DepartmentofMedicalImaging,JinlingHospital,ClinicalSchoolofMedicalCollege,NanjingUniversity,Nanjing,JiangsuProvince,China
X
HuafuChen,
Affiliation:
KeyLaboratoryforNeuroInformationofMinistryofEducation,SchoolofLifeScienceandTechnology,UniversityofElectronicScienceandTechnologyofChina,SichuanProvince,China
X
YuanZhong,
Affiliation:
DepartmentofMedicalImaging,JinlingHospital,ClinicalSchoolofMedicalCollege,NanjingUniversity,Nanjing,JiangsuProvince,China
X
QingJiao,
Affiliation:
DepartmentofMedicalImaging,JinlingHospital,ClinicalSchoolofMedicalCollege,NanjingUniversity,Nanjing,JiangsuProvince,China
X
XingjiangWu,
Affiliation:
DepartmentofGeneralSurgery,JinlingHospital,ClinicalSchoolofMedicalCollege,NanjingUniversity,Nanjing,JiangsuProvince,China
X
[...],
XinxinFan,
Affiliation:
DepartmentofGeneralSurgery,JinlingHospital,ClinicalSchoolofMedicalCollege,NanjingUniversity,Nanjing,JiangsuProvince,China
X
YijunLiu,
Affiliation:
DepartmentofPsychiatry,UniversityofFloridaMcKnightBrainInstitute,Gainesville,Florida,UnitedStatesofAmerica
X
GuangmingLu
Abstract
Background
Minimalhepaticencephalopathy(MHE)isaneuro-cognitivedysfunctioncharacterizedbyimpairmentinattention,vigilanceandintegrativefunctions,whilethesensorimotorfunctionwasoftenunaffected.Littleisknown,sofar,abouttheexactneuro-pathophysiologicalmechanismsofaberrantcognitionfunctioninthisdisease.
Methodology/PrincipalFindings
ToinvestigatehowthebrainfunctionischangedinMHE,weappliedaresting-statefMRIapproachwithindependentcomponentanalysis(ICA)toassessthedifferencesofresting-statenetworks(RSNs)betweenMHEpatientsandhealthycontrols.FourteenMHEpatientsand14age-andsex-matchedhealthysubjectsunderwentresting-statefMRIscans.ICAwasusedtoidentifysixRSNs[dorsalattentionnetwork(DAN),defaultmodenetwork(DMN),visualnetwork(VN),auditorynetwork(AN),sensorimotornetwork(SMN),self-referentialnetwork(SRN)]ineachsubject.GroupmapsofeachRSNwerecomparedbetweentheMHEandhealthycontrolgroups.PearsoncorrelationanalysiswasperformedbetweentheRSNsfunctionalconnectivity(FC)andvenousbloodammonialevels,andneuropsychologicaltestsscoresforallpatients.Comparedwiththehealthycontrols,MHEpatientsshowedsignificantlydecreasedFCinDAN,bothdecreasedandincreasedFCinDMN,ANandVN.NosignificantdifferenceswerefoundinSRNandSMNbetweentwogroups.ArelationshipbetweenFCandbloodammonialevels/neuropsychologicaltestsscoreswerefoundinspecificregionsofRSNs,includingmiddleandmedialfrontalgyrus,inferiorparietallobule,aswellasanteriorandposteriorcingulatecortex/precuneus.
Conclusions/Significance
MHEpatientshaveselectiveimpairmentsofRSNsintrinsicfunctionalconnectivity,withaberrantfunctionalconnectivityinDAN,DMN,VN,AN,andsparedSMNandSRN.OurfMRIstudymightsupplyanovelwaytounderstandtheneuropathophysiologicalmechanismofcognitionfunctionchangesinMHE.
Citation:
QiR,ZhangLJ,XuQ,ZhongJ,WuS,etal.(2012)SelectiveImpairmentsofResting-StateNetworksinMinimalHepaticEncephalopathy.PLoSONE7(5):
e37400.doi:
10.1371/journal.pone.0037400
Editor:
KeweiChen,BannerAlzheimer'sInstitute,UnitedStatesofAmerica
Received:
December26,2011;Accepted:
April19,2012;Published:
May25,2012
Copyright:
©2012Qietal.Thisisanopen-accessarticledistributedunderthetermsoftheCreativeCommonsAttributionLicense,whichpermitsunrestricteduse,distribution,andreproductioninanymedium,providedtheoriginalauthorandsourcearecredited.
Funding:
ThisworkwassupportedbythegrantsfromtheNaturalScientificFoundationofChina[grantno.30700194forLJZgrantno.61125304forHC,grantno.30971019forQJ]andtheNaturalScientificFoundationofJiangsuProvince[grantno.BK2007572forLJZ].Thefundershadrolesinstudydesign,datacollectionandanalysis,decisiontopublish,orpreparationofthemanuscript.
Competinginterests:
Theauthorshavedeclaredthatnocompetinginterestsexist.
Introduction
Hepaticencephalopathy(HE)isacommonandseriousneuro-cognitivedysfunctioninpatientswithacuteandchronichepaticdysfunction,whichischaracterizedbyawidespectrumofclinicalmanifestations,rangingfromalterationsofpsychometricperformancetostuporandcoma[1],[2].Thetermminimalhepaticencephalopathy(MHE)isusedtoclassifyasubpopulationofcirrhoticpatientswithnoobviousclinicalmanifestationbutcanbeidentifiedwithneuropsychologicalexamination,suchasthenumberconnectiontestandthedigitsymboltest[3],[4].MHE,withtheprevalencevariedbetween30%[5]and84%[6]incirrhosispatients,hasadetrimentaleffectonhealth-relatedqualityoflife[7],[8],[9],andhassomepropensitytothedevelopmentofclinicalHE.Inpreviousbehavioralstudies,MHEwasfoundtoprominentlyaffectthecognitionfunctioninthedomainofattention,vigilanceandintegrativefunctions,whilethesensory-motorareaswereoftenunaffected[7],[9].However,theexactpathophysiologicalmechanismsofthesecognitionfunctionchangesinMHEpatientsremainunclearsofar.
FunctionalneuroimagingplaysanimportantroleinuncoveringfunctionalabnormalityofthebraininMHEpatients.Positionemissiontomography(PET)andsingle-photoemissioncomputerizedtomography(SPECT)studieshavedemonstratedthatMHEpatientsexhibitedabnormalitiesinrestingcerebralbloodflowandcerebralmetabolicrateofglucoseandammoniainmanybrainregions,especiallyinfrontalandparietalcortices[10],[11].Twopriortask-statebloodoxygenationleveldependent(BOLD)functionalMRI(fMRI)studiesshowedthattheMHEpatientsexhibitabnormalbrainactivationwhenperformingthetask.Inthefirstreport,Zafirisetal.[12]firstanalyzedtheneuralmechanismsofninenon-manifestHEpatientsusingthecriticalflickerfrequency(CFF)test,andfoundanearly-impairedandcompensatoryneuralmechanismduringvisualjudgmentinthesepatients.Additionally,Zhangetal.observedanabnormalcognitivecontrolfunctioninagroupofcirrhoticpatients(halfwithMHE),usingamodifiedChineseStrooptask[13].
Recently,fMRIstudieshaveindicatedthatthepathophysiologyofmanyhumanbraindiseasessuchasHEmaybeassociatedwiththechangesofspontaneouslow-frequency(<0.08Hz)BOLDfluctuationsmeasuredduringarestingstate.SinceBiswaletal.[14]showedthatspontaneouslow-frequencyfluctuationishighlysynchronousamongbilateralmotorcortices,abnormalsynchronizationhasbeenreportedinmanymentaldiseasessuchasAlzheimer'sdisease[15],[16]andattentiondeficithyperactivitydisorder(ADHD)[17].Arecentworkusingindependentcomponentanalysisrevealedreducedrestingstatesynchronizationbetweendefaultmodenetworkinoverthepaticencephalopathypatients[18].Infact,theeffectsofHEmaybemoreglobal[2],however,whetherotherbrainnetworksarealsoaffectedbyhepaticencephalopathyhasnotbeenfullyelucidatedpreviously.Basedonthefindingsinotherneurologicaldiseasesthatabnormalresting-statebrainnetworks(RSNs)alreadyexistintheearlystageofdisease,e.g.,inearlyAlzheimer'sdisease[19],wehypothesizedthatRSNsmayalsobemodifiedinthemildestformofhepaticencephalopathy-MHE.Inaddition,inmanypreviousPETorfMRIstudies,abnormalitiesofbrainregionsdevotedtoattention,socialcognition,andvisionfunctionswerefoundinMHEpatientsascomparedtohealthycontrols,whilethesensory-motorareaswereoftenunaffected[12],[13],[20].SooursecondhypothesisisthataberrantRSNsofMHEmaymainlyoccurinnetworksassociatedwithattentional,socialcognitionalandvisualprocessing,whilethesomato-motornetworkislittleaffected.
Totestourhypotheses,weadoptedindependentcomponentanalysis(ICA)toinvestigatethechangesoffunctionalconnectivity(FC)ofRSNsin
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