1282 MINERVAANESTESIOLOGICA November2012
These factors may greatly affect the feasibilityof lung disease investigation. Thanks to someuniquefeaturesandgrowingscientificevidence,lung ultrasound (LUS) represents an emergingtechnique for bedside chest imaging in criticalcare. Additionally, with the recently publishedconsensus statementby the InternationalCon-sensus Conference on Lung Ultrasound (ICC-LUS 3 promoted by WINFOCUS, the WorldInteractiveNetworkFocusedonCriticalUltra-Sound), thenomenclature, techniques, and in-dicationsforLUShavebeenstandardized.WhiletheusefulnessofLUSintheemergencysettingis
In thepast25years, imaginghas fostered anunderstandingoflungdiseaseinthecritically
ill1andcurrentlyservesasatooltodiagnoselungpathology,monitor its course, andguide clini-calmanagement.2EverypatientadmittedtotheICU,whatevertheillness,usuallyrequireschestimaging.Availablemodalitiestodayincludetheplain radiograph and the gold-standard CT-scan,alongwithmoresophisticatedtechniqueslikepositronemissiontomographyandelectricalimpedancetomography.Thechoiceofmodalityisbasednotonlyonthespecificindication,butalso on local resources and patient condition.
E X P E R T O P I N I O N
LungultrasoundintheICU:fromdiagnosticinstrumenttorespiratorymonitoringtool
G.VIA1,E.STORTI2,G.GULATI3,L.NERI2,F.MOJOLI1,A.BRASCHI1
1FirstDepartmentofAnesthesiaandIntensiveCare,IRCCSPoliclinicoSanMatteoFoundation,UniversityofPavia,Pavia,Italy;2GeneralICU,AziendaOspedalieraNiguardaCa’Granda,Milan,Italy;3DepartmentofAnesthesia,CriticalCare, and Pain Medicine, Beth Israel Deaconess Medical Center, Boston, MA - Harvard/MIT Division of Health,Sciences,andTechnology,HarvardMedicalSchool,Boston,MA,USA
Anno: 2012Mese: NovemberVolume: 78No: 11Rivista: MINERVA ANESTESIOLOGICACod Rivista: Minerva Anestesiol
Lavoro: titolo breve: Lung ultrasound in the ICUprimo autore: VIApagine: 1282-96
A B S T R A C TImaginghasgreatlycontributedtotheunderstandingoflungdiseaseinthecriticallyillandcurrentlyservesasatooltodiagnoselungpathology,monitoritscourse,andguideclinicalmanagement.Lungultrasoundisareal-time imaging modality that is simple, non-invasive, potentially ubiquitous, and free of ionizing radiation. Itsincreasingpopularityandsupportingresearchdatasubstantiateitsroleasanemergingtechniqueforbedsidechestimagingincriticalcare.Furthermore,theInternationalConsensusConferenceonLungultrasound(ICC-LUS)promotedbytheWorldInteractiveNetworkFocusedonCriticalUltraSound(WINFOCUS)recentlystandard-izedthenomenclatureandtechniqueforlungultrasound,andprovidedrecommendationssupportingitsuseinclinicalpractice.Whiletheutilityoflungultrasoundintheemergencysettingisunquestioned,itspotentialroleinthemorecomplexandresource-richintensivecareenvironmentisstillunderinvestigation.Thepurposeofthispaperwastodescribecurrentandpotentialusesoflungultrasoundinthespecificsettingofadultintensivecare,withanemphasisonrespiratorymonitoring,andtoprovideaframeworkforthepracticalapplicationofthistoolatthebedside.(Minerva Anestesiol 2012;78:1282-96)Key words: Thorax-Lung-Ultrasonography.
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Vol.78-No.11 MINERVAANESTESIOLOGICA 1283
imageoflungtissueisgenerated.Thus,theabil-itytogeneratereal imagesof lungparenchymaalwaysindicatespathology.Ontheotherhand,in cases where air is present in the underlyingparenchymadifferenttypesofimageartefactsareproduced.Differentartefactsrepresentnormallyaeratedlungtissueorrathertissuewithdimin-ishedrelativeaeration,whateverthespecificun-derlying pathological process. Relative aerationmay,infact,bediminishedeitherbylossofair,(developingatelectasis),orbyanaccumulationoffluidorcellsintheinterstitialoralveolarspac-es (pneumonia,contusion,oedema,fibrosis,oralveolitis).
Thegenerationofultrasoundartefactsbyaer-atedlungtissueistheresultofsoundwavereflec-tionandreverberation.Bothphenomenaorigi-natefromthehigh-acousticimpedanceinterfacebetween pre-pleural “watery” tissues and theaerated lung.Thephysical siteof this interfaceisrepresentedbythepointofcontactofthepa-rietalandvisceralpleurallayers.Itappearsultra-sonographicallyasahyperechoictransverseline(the“pleuralline”)locatedbetween,anddeeptotheribs(Figure1A).Sincenearlyallultrasoundwavesarereflectedatthis level,visualizationofanything real is impossible beyond the pleurallayers.However,different typesof artefacts aredisplayedonthefarsideofthepleuralline,gen-eratedbythebouncingoftheultrasoundbeambetween this specular reflector and the probe(reverberation artefacts). The specific featuresof these artefacts vary according to the physi-calpropertiesofthereflector,whichareinturndeterminedbythestateofaerationofthelungimmediately beneath the visceral pleura. Threesituationsmayoccur:1)normallyaeratedlung-generatesahomogeneousreflectingsurfacethatyieldstransverseartefactsparalleltothepleuralline (“A lines”, (Figure 1A); 2) partial loss ofaeration-duetofluidorcellsinsubpleurallungtissue, generates discrete microscopic 3-dimen-sional aerated structures (aerated alveoli/acinasurrounded by fluid or cells); in these circum-stancesair/fluidinterfacesactasspecularreflec-tors,discretefociofreverberation,yieldinglon-gitudinal laser-like artefacts (“B-lines”, (Figure1C)4,5;3)completeabsenceofairbeneaththevisceralpleura(inareasofconsolidation,evenif
clear,itspotentialroleinthemorecomplexandresource-rich intensivecareenvironment is stillunderinvestigation.Thismanuscriptrepresentsan ICC-LUS-conforming 3 description of cur-rent andpotential applicationsofLUS specifictotheadult intensivecaresetting,withafocuson respiratorymonitoring. It alsoprovides theintensive care physician with a framework forthepracticalimplementationofthistoolatthebedside.
Methods
A systematic literature search (January1990-January 2012) on LUS was performedtogatherthemostrecentevidenceonthetop-ic.Termsused invariouscombinations for thesearches on the National Library of MedicineMedline,Cochranelibrary,GoogleScholar,andEmbasedatabaseswere:lung,chest,pulmonary,thoracic, pleural AND sonographic, sonogra-phy, ultrasonographic, ultrasonography, ultra-sound,echographic,echography,ANDbedside,point-of-care.InitialsearchesidentifiedN.=305articles.OnlypapersdescribingsequentialLUSassessment and/or studying adult ICU popu-lations (N.=57) were further selected as coresourceofdataforthemanuscript.Whereappli-cable, recommendations from the recent ICC-LUS 3 regarding indications, terminology, andtechnique were considered. Evidence was sup-plemented with experts’ opinion and personalclinicalexperience.
Fundamentals of lung ultrasound
LUSprovidesarepresentationofthelungthatis based both on images and on artefacts. Thekey factor determining the appearance of theimaged area is the relative amountof air lyingbeyondthevisceralpleura.Sincesonographyisareal-time,dynamicimagingtechnique,LUSof-fersinstantaneousinsightbothintothestateofaerationofthelungandintoitsventilation.
Thestate of aeration oflungparenchymaisameasureofits“air/fluidratio.”Thisratiodeter-minesthecharacteristicsoftheimageproducedbyLUS.Inareasofcompleteconsolidation(thatis,wherethereiscompleteabsenceofair),areal
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Figure1.—Synopsis of lung ultrasound semiotics. Mainsegmentalpatternsareillustrated(leftcolumn)anddescribedintheirdis-tinctivefeatures(rightcolumn). Normalpattern(1A),sonographicinterstitialsyndrome(>3B-lines/intercostalspace)(1C)andpneumothorax(1F)aremutuallyexclusiveartefact-basedpatterns.Pleuralsliding(1A)andlungpulse(1B)arerepresentationsofvisceralpleuralmotion(inaventilatedandanonventilatedlungarea,respectively),andarehereshownusingM-Modeimagingashavingadifferentappearanceofartefactsbeyondthepleuralline.M-Modeprovidesrepresentationovertimeofreflectedechoesfromasinglescanningline:structuresperpendiculartotheultrasoundbeamarerepresentedbydotsataspecificdepthandap-pearasstraightlineswhenmotionless.Effusion(1C)andconsolidation(1D)areimage-basedpatterns,andtheirinterpretationismoreintuitive3,9foramoreextensivedescription.E:effusion;P:lung;L:liver;S:spleen;e:loculatedeffusion;asterisksindicateribshadows).
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accuracytothefactthatnearlyalllungpatholo-giesrelevanttothecriticallyillhaveaperipheralmanifestation.
Lung ultrasound technique: a shift in concept of lung imaging
In comparison to the overall lung picturedisplayed by routine techniques (monoplane,frontal,with chestX-ray,ormulti-plane, eithercoronal/sagittal/transverse, with CT-scan), LUSprovides multisite regional representations of the lung. The clinician must then reconstruct theoverall three-dimensionalpictureby integratingallsegmentsinhis/hermind.Thiscognitiveproc-essmoreresemblestheinterpretationofausculta-tionfindingsratherthaninterpretingtheimagesprovidedbyCTor aplain radiograph.Fromapractical point of view, a LUS examination in ICU patients should systematically investigate six areas of interest per side,dividingeachhemithoraxintoananterior,lateral,andposteriorregion(ac-cordingtoanatomicallandmarksrepresentedbyaxillarylines),andeachregionintoanupperandlower region (Figure 2). Scanning the patient’sposteriorregionsjustdorsaltotheposterioraxil-larylinewithminimalpatienttiltingmaymanytimessuffice.Notethattheposteriorportionsofupperlobesareoftenblindspots.Theexamina-tioncaneitherbecomprehensive —every inter-costalspaceisentirelyscanned10—orsimplified — one representativepointper area is scanned11(similartothesimplifiedapplicationofotherimagingmodalitiesonclinicalgrounds12).Thetimerequiredcanthusrangefrom5to15min-utes.Inthesimplifiedapproach,ifanabnormal-ity is identified, inspection is further extendedtodefineitsboundaries.Forthepurposeoflungaerationquantification(seebelow),themostse-verepathologicalfindingcanbeconsideredrep-resentativeoftheentireregion.
The peculiarities intrinsic to LUS imagingdiscussed above require specific tools to aid incommunicationandclinicaluseofexaminationfindings. Archiving and reporting are manda-tory.Simplifiedreportforms,ideallyelectronic,arerecommended(Figure2)fortheireaseofuseand their effectiveness in promoting learningandimplementationofLUSindailypractice.13
small) - restores favorable conditions for ultra-soundtransmissionwithonlypartialreflection,generating a representation of lung tissue as asolidorgan(Figure1E).6
Thestate of ventilationofaeratedscannedar-eas is evidenced by changes in the appearanceofthepleurallineovertherespiratorycycle.Itsrespirophasicshimmering(“lungsliding”3),cor-respondstothecontinuedtoandfromotionofthevisceralpleuraontheparietalpleura,indicat-ingthepresenceofventilationintheinspectedarea.Ontheotherhand,aheart-beatsynchro-nized motion of the pleural line (“lung pulse”7)impliestheabsenceofventilation,asinearlyatelectasis,beforealveolarairresorptionensues.A motionless pleural line (“sliding abolition”)potentially indicates a detachment of the twoviscerallayerswithinterpositionofair.8
Additionally, LUS detects collections in thepleural space that can be further characterizedby specific patterns. These patterns can be ei-therartifactualorimage-baseddependingupontheconstituentsofthepleuralcollection(airorfluid).Inthecaseofagaseouscollection(pneu-mothorax),theslidingabolitioninadependentarea is matched with the inspiratory coming-into-view (seenas the sudden re-appearanceoflung-sliding) of a mobile, partially collapsedlunginamorelateralordorsalsite(thesocalled“lungpoint”8)(Figure1F).Thecombinationofthesetwosignsbasedonartefacts(slidingabo-litionand lungpoint)allows thepositivediag-nosis of pneumothorax.8 In the case of a fluidcollection(pleuraleffusion),animageofvariableechogenicityisgeneratedbetweenthetwopleu-rallayers(Figure1D).
Based on these concepts, a well-defined se-mioticshasbeenvalidated,3andreliesoneasilydistinguishable segmental patterns (Figure 1):normality, sonographic interstitial syndrome,pleural effusion, consolidation, and pneumo-thorax.AdetaileddescriptionofLUSsemiotics,beyondthepurposeof thismanuscript, isout-lined elsewhere.3 9 It may be understood fromthisshortsynopsisthatLUSrelatestothedegreeofaerationofthelung’souter,subpleurallayer.Onlyconsolidationsthatreachthevisceralpleu-ra (and effusions) permit deeper investigation.LUSisasurfaceimagingtechnique,andowesits
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Figure2.—Simplified report form for lung ultrasound in the ICU. Withsimplecheck-boxingandminimaltyping,itallowsforrapidreportingofdiagnostic,screening,monitoringandprocedure-guidanceexaminations.Visualrepresentationofdifferentexploredregions(2anterior,2lateral,2posterior,accordingtoanatomicallandmarkssetbyaxillarylines)andnumber-codedratingoffind-ingsprovideinstantaneousperceptionoftheoveralllungultrasoundrepresentation.Calculationofalungultrasound(LUS)scoreallowssemi-quantificationofthestateofaerationoftheentirelung.Additionalfree-textdescriptionandpresumptivediagnosiscompletethereport.Theexamaminationcanbeconductedinasimplifiedmanner(inspectionatasinglerepresentativepointperregion),ascomprehensiveinvestigation(eachintercostalspaceentirelyinspected,withtheworstfindingperregionconsideredforrating),orevenasafocused,single-regionexamination(forexample,justdorsal,toquantifyaknowneffusion).Forthepurposeofcorrectinterpretation,detailedhistory,clinicalconditions,andventilationarereported.Storagecodeforretrievalofimagesfromanarchiveisindicated.
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bytheappearanceofsub-pleuralconsolidations,whichfinallyenlargedanddeepened,eventuallyencompassingtheentirelung14(Figure3).
The accuracy of LUS in assessing aeration ofthelunghasbeenfurtherdemonstratedincriti-cally illpatients,both in the contextof ventila-tor-associatedpneumonia(VAP)andacute lunginjury (ALI)/acute respiratorydistress syndrome(ARDS).LUS score-quantifiedaerationchangesobservedinVAPpatientsuponinitiationofan-timicrobial therapyshowatightcorrelation withCT-measurementsoflungaeration(Day0vs.Day7);15 scoring was based on a comprehensive 12areaperlunginvestigation,accordingtoprogres-sionorregressionofpatternsof:normality,spacedB-linesand/orsmallsubpleuralconsolidation,co-alescentB-lines,andconsolidation.Whencom-pared with the pressure-volume curve method forassessingPEEP-inducedlungrecruitmentinALI/ARDS,16thesamescorewasaccurateindetectingsignificant increases in lungaeration (>600mL,detectedbyascore≥18).Accuracydiminishesformilder degrees of re-aeration (a 75-450 mL in-creaseisassociatedtoascore≥14).16Thus,turningimages into numbers (semi-quantitation) is thekeytoeffectiveLUSassessmentofchangesintheoverallstateoflungaeration.
At single lungareas,qualitative estimation ofaeration loss with LUS (whatever its etiology) correlateswelltoCTfindings,3andcanbegrad-edas:
1) moderate: multiple, well spaced, B-lines.Thiscorrespondstoaninterstitialprocess(thick-enedinterlobularsepta,as inedema4orfibro-sis,17whichgenerates regularly spacedB-lines),or to an alveolar process (disseminated foci ofpneumonia15orongoing,butnotcompleteyet,atelectasis,14 which generates irregularly spacedB-lines);
2) severe: closely spaced/coalescent B-lines(fluid-filledalveoli).ThiscorrespondstogroundglassopacitiesonCT;18
3)complete:ultrasoundconsolidations.ThiscorrespondstocompletelossofaerationseenonCT.18
In comparison to other bedside techniqueslike the wash in-wash out 19 and the pressure-volume curve methods,20 LUS offers thus theappealingabilitytosemi-quantitativelydescribe
Sometechnicalnotesconcerningprobesandmachinesettingsdeservemention,as theymaygreatly affect LUS findings and interpretation.Asdescribedinthe literature,LUScanbeper-formedwithanyprobe(highfrequency,suchaslinearormicro-convex,or low frequency, suchasconvexorphasedarray).Butdifferentrangeoffrequenciessuitbetterdifferenttargetsoftheultrasound inspection: high frequencies (9-12MHz) visualize at best the pleuras, their anat-omyandlungsliding; lower frequencies(2.5-5MHz)allowbetterappreciationoftheindepthextension of B-lines and of consolidations/ef-fusions.Themicroconvexprobe,with its smallfootprint (fitting into intercostal spaces) anditswiderangeoffrequencies(5-11MHz)isre-gardedbymanyastheidealprobe.9ForacorrectexecutionofLUS examination, specific adjust-mentsofmachinesettingsarerequired:removalof harmonic-imaging and lowering of “reject”postprocessing(whichotherwisediminisharte-facts);eliminationofmulti-focusmodalityandfocussettingatthelevelofthepleuralline;depthsettingat6-7cmfromthepleuralline(forfullappreciationoftheextensionofB-lines);storageclip length set to include an entire respiratorycycle.OthertechnicalissuesspecifictotheICU(ultrasound machine features, disinfection) aredescribedexhaustivelyelsewhere.10
Basis for ultrasound suitability for monitor lung aeration changes
Ease of use, bedside availability, and repeat-ability make LUS particularly suited to detectspatialandtemporalheterogeneityoflungaera-tioninpatientswithrespiratoryfailure,provid-ing key information for their clinical manage-ment.1 A continuum from normally aeratedtissuetocompletelossofaerationexistsinLUSsemiotics,andeachdifferentLUSpatterncorre-spondstoagivendegreeofaeration3.Inhumanstudysubjectssubmittedtoseparatelungventi-lation(amodelofiatrogenicgradualresorptiveatelectasis),14LUScharacterizedthesonographicappearanceoftheprogressivelossofairfromnor-malitytotheappearanceofB-linesandpleuralirregularities, followedby an increase inB-linenumberanddensity.Thiswasinturnfollowed
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—step1:identificationoflandmarks-Iden-tificationofthediaphragm(toappropriatelyat-tributefindingstothechest)andtheintercostalspace (to correctly recognize the pleural line)must be performed before identification of re-gionalultrasoundpatterns(Figure4);
—step2:segmentalassessment-Eachareaofinterest(whetherarepresentativespotinaregionoreachentireintercorstalspace)issonographi-callycharacterized(Figure1).Abinarysequen-tialinterpretationiseasyandeffective(Figure4);
— step 3: overall lung integration (“sono-graphic diagnosis”). Cumulative impressionfromsinglescansistranslatedintotypicallungpatterns (Table I). Recognizing spatial (focal/diffuse, monolateral/bilateral, homogeneous/inhomogeneous)andtemporal(acute/pre-exist-ing, stable/evolving) distribution of ultrasoundfindings is the key to correct interpretation.Potentially associatedpleural abnormalities canprovideimportantclues3,especiallyindifferenti-atingbetweencardiogenicandnon-cardiogenicaetiologies25.Findingsfromallregionsmustbeconsidered,aspartialinterpretationmaybede-ceptive26. IntheICU, incontrast totheemer-gencyroomsetting, limiteddorsal sonographicinterstitialsyndromemaynotberelatedtoanyspecificaetiologyother thantheeffectof long-lastingsupineposition/passiveventilation.AlsointheICU,overlappingdiseaseseasilycoexist;
—step4:in-contextinterpretation(clinical-instrumentaldiagnosis).Itmustbestressedhow
regional aeration as well, rather than only theglobalamountoflungaircontent.14-16However,incomparisontoelectricalimpedancetomogra-phy,21itsuffersthelimitationofprovidingnei-therquantitativenorcontinuousdata.
Lung ultrasound applications in the ICU
Differential diagnosis of respiratory failure
The chest radiograph is often unable to sat-isfactorilyanswerthemostcommondiagnosticquestions about patients with respiratory fail-ure:22,23“Isthereextravascularaccumulationoffluidinthelung?”,“Istheedemacardiogenicornot?”,“Isanimpendingpulmonaryinfectionthepotentialsourceofthisnewsepticstate?”,“Hasthelungde-recruited?”,“Isthisanatelectaticoranalveolarconsolidativeprocess?”.Someques-tionsareevenraisedafterradiographshavebeeninterpreted:“Doesthatopacityrepresentconsol-idation or effusion?”, “Is that a pneumothoraxora false image?”,“Aretherebronchopneumo-niafocibehindtheheart?”.Thesemaybecomecriticalissueswhentime,clinicalconditions,andlogisticburdenhinderaccess toCTscan.LUScharacterizes pleural and lung pathology withhighersensitivityandspecificitythanthecurrentICUbedsidereferencesofauscultationandchestX-ray,1824andasystematic LUS approach 3asout-linedbelow,usuallyprovidesquickexplanationofthecausesoflungfailure:
Figure3.—Sequential lung ultrasound inspection at the same intercostal space (4th, left antero-superior) during iatrogenic atelectasis.Indoublelungventilation,uponexclusionoftheleftlung,repeatedlungultrasoundassessmentshowssignsofprogressivelossofair(AtoE),uptocompletede-aeration.B-lines(B,arrowheads)appear,increaseinnumberandcrowdingtobecomecoalescent,eventuallycreatinga“whitelung”pattern(C,asterisks);pleuralthickeningappears;asmallperipheralconsolidation(C,arrows)becomesvisible;consolidationthenbecomestheprevailingpattern(D,notealsocoalescentB-lines,asterisks,originatingfromitsboundaries);finally,completelungconsolidationensues(E,scanningatincreaseddepthandparalleltotheintercostalspace,tobettershowwholelungextension:notethedescendingaortaisvisibleinitslongaxis,asterisk).
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tern changes in 12 regions of interest,15 LUSaccuratelydescribedaerationchangesrelatedtosuccessfulantimicrobialtreatmentofventilator-associated pneumonia.15AparticularlysignificantcorrelationwasfoundbetweenCTandLUSre-aeration(Rho=0.85,P<0.0001):aLUSscore>5was associatedwith aCT-measured re-aeration>400mLandasuccessfultherapy,whileascore≤-10wasassociatedwitha lossofCTaeration>400mLandafailureoftreatment.15
In cardiogenic pulmonary edema (“wet lung”LUS appearance), the overall number anddensityofB-lines are accuratemarkersof lungcongestion severity. They correlate with chestX-ray findings,29 arterial blood oxygenation,30natriuretic peptide levels,31 transpulmonarythermodilution measured extravascular lungwater,32 and pulmonary capillary wedge pres-
onlyabalancedandpertinentinterpretationofsonographicfindingsinlightofthepatient’shis-tory, clinics, biochemistry, other instrumentaldata, and ongoing treatment will provide thecorrectdiagnosis.Additionally,integrationwithvenous 27 and cardiac ultrasound (in a “wholebodyapproach 9”)has thepotential to reachaveryhighdiagnosticaccuracy.
Monitoring of specific lung diseases
Repeated systematicLUS assessment can ef-fectivelytrackthecourseofpleuralandlungdis-ease in the ICU.3As alreadydemonstrated forconsolidative non-severe community-acquiredpneumonia,28LUSprovidesaccuratefollow-upofpneumoniainICUpatientsaswell.Bymeansofare-aerationscorecalculatedfromLUSpat-
Figure4.—Sequential interpretation of lung ultrasound findings at a single scan area. Eachareaexploredwithultrasoundischar-acterizedtofitintooneofthesegmentalpatternsdescribedinFigure1:normality,sonographicinterstitialsyndrome,effusion,consolidation,orpneumothorax.Uponpreliminaryassessmentoftheadequacyoftheacousticwindowonthelunganddetectionofthelandmarks(recognizableintercostalspaceandpleura),interpretationofthepleuralinterfacecomesfirst:itsdefinitionasfluid-airinterface(yieldingartefacts)orasfluid-fluidinterface(yieldingimages)isakeysteptocharacterizethestateofaerationoftheexploredarea.Assessmentofvisceralpleuralmotion(sliding/nosliding/lungpulse)speakstolungventilation.Artefactsorimagesbeyondthepleuraaretheninterpretedtoyieldafinalsegmentalsonographicdiagnosis.*InB-pattern(sonographicin-terstitialsyndrome,morethan3B-lines/intercostalspace),thepresenceofpleuralthickening/abnormalitiesandsubpleuralsmallconsolidationsfavorsinflammation/de-aerationwhileasmoothnon-thickenedpleurafavoursincreasedextravascularlungwater.**Differentialdiagnosisbetweenpoorlyechogenicconsolidationsandeffusionmaynotalwaysbeeasy:afluctuatingappearanceofthefarboundaryofthelesion(representedbyM-Modeasthe“sinusoidsign”9)standsforfreefluid(effusion);anirregular,raggedfarborderofthelesion(the“shredsign”9)representsthedeepboundaryofconsolidation,thejunctionbetweenconsolidatedandaeratedparenchyma.Lobarconsolidationshaveinsteadaregularboundary,butrarelyahypoechoicappearance.
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Suspectedcauseoflungfailure Hallmark Extension Distribution Pleuralfeatures
Normal lung(as reference)
“APattern”*(DorsalB-PatternfrequentinICU)
Diffuse Bilateral,symmetrical
Thinpleura,sliding
Pneumonia,Broncho-pneumonia
Consolidationtissue-likeorhypoechoic(earlyessudativephase)texture,w/irregular,blurredmargins+dynamicairbronchogramsorfluidbronchograms
Focal,multifocalDorsal(>frequent)Anterior/Lateral(possible)
Monolateral(atonset);bilateral,asymmetrical(Ifevolving)
N/A
Sono-interstitialsyndrome(B-Pattern)(interstitialpneumonia)IrregularlyspacedB-lines
Focal,multifocalAnterior/Lateral/Dorsal
Monolateral(atonset);bilateral,asymmetrical(Ifevolving)
Pleuralabnormalities(thickened/fragmentedpleura,subpleuralconsolidations)ifB-PatternReducedsliding/Nosliding/lungpulse
Atelectasis ConsolidationwithregularmarginsNodynamicbronchograms
FocalAnterior/Lateral/Dorsal
Monolateral N/A
AorBpattern(ongoingatelectasis)
Focalanterior/lateral/dorsal
Monolateral Lungpulse
Hydrostatic/Cardiogenic
PulmonaryEdema
Sono-interstitialsyndrome(B-pattern)RegularlyspacedB-Lines(septaledema)Crowded/coalescent(alveolaredema)
DiffuseAntero-lateral(untreated,acutephase)Lateral(treated,subacute)*DonotconsiderDorsal(misleadinginICU)Gravitygradient
Bilateral,symmetricalHomogeneous
Smooth/non-thickenedpleurallinePreservedsliding
ALI/ARDS Sono-interstitialsyndrome(B-pattern)IrregularlyspacedB-linesConsolidationsDorsal
DiffuseUnrelatedtogravity
Bilateral,symmetricalInhomogeneous(patchydistribution,“sparedareas”)
Pleuralabnormalities(thickened/fragmented,anteriorsubpleuralconsolidations)ReducedslidingLungpulse
LungContusion Sono-interstitialsyndrome(B-pattern)(atonset)irregularlyspacedB-linesConsolidation(evolving)
Focalmultifocal
Monolateralbilateral,asymmetrical
Pleuralabnormalities(thickened/fragmented,subpleuralconsolidations)Preserved/reducedSliding/lungpulse
Alveolitis Sono-interstitialsyndrome(B-Pattern)
Diffuse
Bilateral,symmetrical
Pleuralabnormalities(thickened/fragmented)Preserved/reducedsliding
TableI.—Differential diagnosis of potential causes of lung failure in the ICU.
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with severity inALI/ARDS aswell.1634 Interest-ingly, in an experimentalmodel ofALI, a tightcorrelationwasfoundbetweenthenumberofB-linesandthegravimetry-measuredwet/dryratioofthelungtissue.39LUSevaluatesthetimecourseandresponsetotreatmentofALI/ARDS40,41byreliably tracking aeration andextravascular lungwater changes upon PEEP titration,16 recruit-mentmaneuvers,pronation,42lungre-expansionafterpleuraldrainage,andnegativewaterbalance.
Theamountofapleural effusioncanbeaccurate-lydeterminedwithLUS,eithersemi-quantitatively43, 44 or quantitatively.45 One can also monitortheclinicalcourseofapleuraleffusionandtrackitsresponsetomedicaltreatment.46Thisabilitytomonitorpleuralcollectionsisespeciallyimportantinthesettingofstablepatientswithchesttrauma,asinthesesettingsitmaybemoreappropriatetoclosely follow the evolution of hemothoraces orpneumothoracesratherthantodrainthemimme-diately.Inparticular,thesuperficialextensionofa
sure.32,33TheclinicalobservationthatLUSisamoresensitivemeansfordetectingextravascularlung water variations when compared to chestX-rayor auscultationmatcheswithfindings inananimalmodelofinflammatoryedema,whereB-linesappearedevenearlierthanadecreaseinarterial oxygen tension.34 Moreover, favorableresponsetotreatmentisassociatedwithprogres-sive, real-time, reduction in the number of B-lines,uptotheircompleteclearance,asdemon-stratedwithcontinuouspositiveairwaypressure/non-invasiveventilation35,36andfluidremovalbymeansofdiuretics14,35anddialysis.37,38Ev-idence supports the use of LUS as a point-of-care,real-time,simpletooltodirectlyimageandmonitorextravascularlungwater.3Additionally,detectionofanoverallLUSpatternof“drylung”(antero-lateralnormalpattern)suggeststhatini-tialfluidloadingmaybegivenwithoutconcernforhydrostaticpulmonaryedema.33
ThenumberandcrowdingofB-linescorrelates
Suspectedcauseoflungfailure Hallmark Extension Distribution Pleuralfeatures
Pulmonaryfibrosis Sono-interstitialsyndrome(B-Pattern)
Diffuse(>dorsallowerlobes)
Bilateral,symmetrical Pleuralabnormalities(thickened/fragmented,subpleuralcysts)Preserved/reducedsliding
Pneumothorax Pneumothorax(A-Pattern+LungPoint)
Focal Usuallymonolateral Nosliding
Pleuraleffusion Intra-pleuraanechoiccollection(transudate)Echogenic,particulatedincomplexeffusion(exudate,blood)Maybeseptated(exudate)
N/A Monolateral,bilateral N/A
Pulmonaryinfarction Consolidations,2/more,Small(1-3cm)Echo-poor,wedge-shaped
Focal>Dorsal(>rightlowerlobe)
Monolateral(atonset);bilateral,asymmetrical(ifrepeated)
N/A
COPDexhacerbation,asthma
A-pattern Diffuse Bilateral,symmetrical PreservedslidingReducedsliding(hyperinflation)
COPD:chronicobstructivepulmonarydisease.
TableI.—Differential diagnosis of potential causes of lung failure in the ICU.
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is not surprising to observe that exploring thelung directly with the same technology yieldsevenmoreinformation.41LUShasthepotentialtopredict lungrecruitabilitybasedonobserva-tionsoflungmorphology,whichisakeypredic-tor of the response to recruitment maneuvers.48Early-stagefocuseddistributionofaerationloss(a state associated with poor recruitability andmajorrisksofoverdistentionofaeratedregions)is representedby anearlynormalLUSpatternorapaucityofB-linesinantero-lateralareasandconsolidation or crowding of B-lines in dorsalones.Ontheotherhand,early-stagediffusede-
pneumothoraxcanbemappedandmonitoredac-cordingtothelaterallocationofthelungpoint(s).8
Lung-related procedures and their monitoring
A wide range of bedside procedures per-formed on critical respiratory disease patientsbenefit from information provided by lungimaging. As such, many of them represent ei-ther established or potential applications ofLUS.Sinceultrasonographicinvestigationoftheheartisacknowledgedasakeytoolintheventi-latorymanagementofALI/ARDSpatients,47 it
Figure5.—LUS changes in dependent areas upon pronation in an ARDS patient.Left(upperpanels)andright(lowerpanels)showsequential dorsalscansinanARDSpatientsubjectedtopronationonday3ofdiseasecourse.Inbothareasofinvestiga-tion,LUSfindingsshiftedfromapatternofconsolidation(6Aand6C,arrows)toaB-patternontheleft(6B)andanearlynormalpattern(6D:justoneB-line,arrowhead)ontherightside.Timeelapsedbetweenthe2sequentialacquisitionswas30minutes.
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sound-aidedmanagementofpleural effusions infebrileICUpatientsalsohastensdiagnosisandag-gressive treatment of empyema.54 Pneumothorax drainage with LUS guidance has utility only inthelife-threateningscenarioofhypertensivepneu-mothorax,sinceultrasoundcanonlydiagnosethepresenceofintra-pleuralaircollectionsandsurfaceextension,but cannot gauge theirdepth.8How-ever,LUScanbeusedeffectivelyforpneumothorax follow-up.TheaccuracyofLUSfordetectingresid-ualpneumothoraxafterdrainageandfordefiningthetimingforchesttuberemovalisgreaterthanthatofchestX-ray.55
Assessment of weaning from mechanical ven-tilation.—LUS has been shown to be useful inmonitoring and managing the weaning process from mechanical ventilation. Firstly, it allows for de-tection and treatment of obstructive atelectasis,de-recruitedareas,andrelevanteffusionssoastooptimize the starting conditions for extubationandspontaneousbreathing.56Furthermore,LUSprovidesinformationthatcanbeusedtopoten-tiallypredictthesuccessorfailureofaspontane-ousbreathingtrial(SBT).Bymultisitequantifi-cation with a LUS four-tiered score (0=normalpattern; 1=multiple spaced B-lines; 2=multiplecoalescent B-lines; 3=consolidation) the state oflungaerationbeforetheSBTandtheamountofde-recruitment after the trial can be described.Higherscoresaredetectedinpatientsmorelikelytosubsequentlydeveloppost-extubationrespira-tory distress.57 The LUS score at the end of anSBTpredictspost-extubationdistresswithanareaunder the ROC curve of 0.86, 95% CI (0.79-0.93), with 0.82 sensitivity and 0.79 specificityforaLUSscore>14,abetterperformancethanplasma BNP values and echocardiographic-de-rivedparameters.ALUSscoreatendSBTof≤12or >17 accurately identifies patients with a loworhighlikelihoodofpostextubationdistress,re-spectively.57Asanaccuratetoolforthedifferentialdiagnosisofcardiogenicandobstructivecausesofrespiratoryfailure,58LUSmayalsoallowpromptrecognitionofacardiogeniccomponentofacutepost-extubationrespiratorydistress.
Finally,diaphragm ultrasonography, easilyob-tainedduringLUSscanningoflowerquadrants,provides additional insights on tolerance toweaning. Preliminary studies in cohorts of pa-
aerationisassociatedwithamorehomogeneousinterstitial pattern characterized by coalescentB-lines.However,hyperinflation cannotbe ac-curately diagnosed with LUS, even if one ob-servesmarkedlyreducedslidinginthecontextofanormalLUSpattern.LUSfindingscannotbeusedinisolationtodetermineappropriatePEEPsettings.Alongwiththeoverallclinicalpicture,LUScansupportthechoiceofpronation(ifdor-salconsolidationsprevail)andmonitoritseffectsinreal time 42(Figure5).Veryempirically,buteffectively,detectionofderecruitedareaseveninlessseverecontextsthanALI/ARDSallowsop-timizationofventilatorystrategy,49forexample,bymeansofpostural therapy,orinthechoiceofusingnon-invasiveventilationratherthanCPAPinspontaneouslybreathingpatients.
Byhelpingtheintensivistrecognizetheatelec-tatic nature of a consolidated area (absence of a“dynamicairbronchogram”orpresenceof“fluidbronchogram”,28positivepredictivevalue94%6),LUScansuggesttheneedtorestorebronchuspa-tencybymeansoffiberoptic bronchoscopy.Whenadistal airway specimenisindicatedbythesuspicionofpneumonia,LUScanidentifythebestlobetotarget,50 with higher accuracy than chest X-ray.Management of pleural effusions,whatevertheset-tingorthepurpose,isgreatlyaidedbyLUS.Thedecisiontoperformpleuraldrainage isbasedonestimatingthepotentialcompressiveeffectoftheeffusion,whichdependsonthevolumeoftheef-fusion.LUScanestimatepleuraleffusionvolumesemi-quantitatively (an expiratory inter-pleuraldistanceatthethoracicbase>45-50mmor>50mmaccuratelypredicts >800mL 43 or500mL44effusions,respectively)orquantitatively(multi-planeapproach,basedontheeffusionlengthtimesmid-heightareaformula).45Theseestimatestight-lycorrelatewithCT-scanestimatesandcollectedfluid volumes. The procedure itself is optimizedbyidentifyingthemostdependentandsafestsiteof puncture 51 andbymonitoring the results ofthethoracentesisinreal-time.Furthermore,LUShasshownsuperioritytostandardchestX-rayandCT-scanincharacterizingtheinternalcomplexityofaneffusion:52detectionofcomplexseptatedorcomplexnon-septated effusions (internal echoes,mobile particles), as in hemothorax/empyema,cansuggesttheuseofchest tube drainage.53Ultra-
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difficult to master (for example pneumothoraxconfirmation).67
Lung ultrasound nevertheless suffers manylimitations.Themainlimitationsarebasedonanoverall lowerdiagnosticaccuracy thanCT-scan(especially concerning precise quantification oftheextensionoflunglesionsanddeeperlesionswithoutconsolidation/effusion),inabilitytoim-ageparavertebralregions(beneaththescapulae),and hypo-echogenicity of some patients (withobesity, wounds/dressings, tissue edema). EventhoughLUScanprovideanaccuratesemi-quan-titative assessment of lung aeration, it cannotevaluatehyperinflation,arelevantissueinALI/ARDSpatientsmanagement.68
The issue of infection transmission via the ul-trasoundprobealsodeservesattentionandfurtherinvestigation.69Finally,aswitheverynoveltool,im-plementingLUSrequiresanorganizedward/depart-menteffortwithastandardizedapproach,commonlanguage,anduniformstafftraining.Atthistime,thesystematicuseofLUSinICUsisstillscarceincomparisontothefieldofemergencymedicine.
LUS has the potential to become a referencetool forbedsidedynamic respiratorymonitoringintheICUandcanfilltheimage-resolutiongapbetweenchestradiographsandCT-scans.Contin-uedresearchisneededtoplaceLUSinevidenced-baseddiagnosticimagingstrategiesandimplementitintogoal-directeddiagnosisandmonitoring.
Key messages
— Lung ultrasound quickly provides atthebedsiderelevantinformationonthestateofaerationandventilationofthelung.Ithasthecapabilitytodescribespatialandtempo-ralheterogeneityoflungaerationandextra-vascularlungwatercontent.
—Lungultrasound can track effectivelythecourseoflungandpleuraldiseaseintheICUandguide several aspectsof theman-agementofrespiratoryfailure.
—Inthehandsofadequatelytrainedphysi-cians,lungultrasoundhasthepotentialtofilltheimage-resolutiongapbetweenchestradio-graphsandCT-scans,andtogreatlycontributetobedsiderespiratorymonitoringintheICU.
tientsscheduledforextubationshowedthatonecouldidentifypatientsathighriskofdifficultyweaning during an SBT (M-Mode measureddiaphragmatic descent <10mm correlates withhigher rates of primary, 83% vs. 59% P=0.01,and secondary weaning failure, 50% vs. 22%P=0.01).59 Furthermore, a cut-off value forspleenandliverdownwarddisplacementof>11mm can predict successful extubation (84.4%and82.6%sensitivityandspecificityrespective-ly,betterthantraditionalweaningparameters).60Inanotherstudy,theworkofbreathingwasin-directlyestimatedinextubatedpatientsathighriskforfailuresubjectedtoplannednon-invasiveventilation. Investigators found an inverse cor-relationbetweenfractionaldiaphragmaticthick-eninginthechestwallappositionzoneandthepressure support level (spontaneous breathingvs.5cmH2Oincrementalsteps,P<0.05).61LUSevenhasthepotentialtomonitorrecoveryfromdiaphragmaticweaknessorparalysis.62
Advantages and limitations of lung ultrasound
Knowledge gaps and future directions
LUShasmanyappealing features thatmakeits application in the ICUpotentially advanta-geous. It uses basic technology (only 2D andM-Modecapabilitiesarerequired)andisfreeofionizingradiation.Itisalsonon-invasive,repeat-able,cost-effective,63andintrainedhands,moreaccuratethanthebedsidelungimagingalterna-tive,chestX-ray.18,24Moreover,unlikeCT-scan,LUSdoesnotrequirethepatienttransportout-side theunit.Moresubtly, thanks to thereadyavailabilityofLUSintheclinician’shands,pa-tients may benefit from a lower threshold forperforming the ultrasound examination thanfororderinganalternativetest.Therefore,earlierand more frequent lung investigations may betheconsequenceofLUSuse.Furthermore,sinceimage-based patterns are intuitively recognizedandartifactualonesaremutually exclusive (in-terpretationproceedsinabinaryfashion,Figure4),LUS technique is largelyoperator-indepen-dent, in contrast to other ultrasound applica-tions.3164-66Still,appropriatetrainingiscrucial,especiallyforthoseLUSdiagnosesthataremore
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20. Lu Q, Constantin JM, Nieszkowska A, Elman M,VieiraS, Rouby JJ. Measurement of alveolar derecruitment inpatientswithacutelunginjury:computerizedtomographyversuspressure-volumecurve.CritCare2006;10:R95.
21. MudersT, Luepschen H, Zinserling J, Greschus S, Fim-mers R, Guenther U et al.Tidal recruitment assessed byelectricalimpedancetomographyandcomputedtomogra-phyinaporcinemodeloflunginjury.CriticalCareMed2012;40:903-11.
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24. XirouchakiN,MagkanasE,VaporidiK,KondiliE,PlatakiM,PatrianakosA et al.Lungultrasoundincriticallyillpa-tients: comparisonwithbedsidechest radiography. Inten-siveCareMed2011;37:1488-93.
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26. VolpicelliG,NobleVE,LiteploA,CardinaleL.Decreasedsensitivityoflungultrasoundlimitedtotheanteriorchestin emergency department diagnosis of cardiogenic pul-monaryedema:aretrospectiveanalysis.CritUltrasoundJ2010;2:47-52.
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35. Volpicelli G, Caramello V, Cardinale L, Mussa A, Bar F,FrasciscoMF.Bedsideultrasoundofthelungforthemoni-toringofacutedecompensatedheartfailure.AmJEmMed2008;26:585-91.
36. Liteplo AS, Murray AF, Kimberly HH, Noble VE. Real-time resolution of sonographic B-lines in a patient withpulmonaryedemaoncontinuouspositiveairwaypressure.AmJEmMed2010;28:541e5-8.
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Thi
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is p
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by
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iona
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No
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aut
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rson
al u
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o do
wnl
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and
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onl
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s A
rtic
le.I
t is
not
per
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o m
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addi
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(eith
er s
pora
dica
lly o
r sy
stem
atic
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, ei
ther
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or e
lect
roni
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rtic
le fo
r an
y pu
rpos
e.It
is n
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to
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e th
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ectr
onic
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the
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thr
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and
/or
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anet
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sha
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syst
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or a
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Art
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.The
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all o
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e A
rtic
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of d
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ReceivedonJanuary19,2012-AcceptedforpublicationonJuly20,2012.Correspondingauthor:G.Via,FirstDepartmentofAnesthesiaandIntensiveCare,IRCCSPoliclinicoSanMatteoFoundation,UniversityofPavia,piazzaleGolgi2,27100Pavia,Italy.E-mail:gabriele.via@winfocus.orgThisworkisfreelyavailableatwww.minervamedica.it
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ctio
n is
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horiz
ed.I
t is
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mitt
ed fo
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rson
al u
se t
o do
wnl
oad
and
save
onl
y on
e fil
e an
d pr
int
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y of
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s A
rtic
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t is
not
per
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o m
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(eith
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or e
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roni
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thr
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onl
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and
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.The
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