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w w w . j c o l . o r g . b r

Journal

of

Coloproctology

Original

Article

CT

enterography

in

the

evaluation

of

Crohn’s

disease

Carlos

Henrique

Marques

dos

Santos

a,∗

,

Jovino

Nogueira

da

Silva

Menezes

b

,

Thiago

Franchi

Nunes

c

,

Letícia

de

Assis

Martins

c

aServiceofColoproctology,HospitalUniversitárioMariaAparecidaPedrossian,CampoGrande,MS,Brazil bServiceofGeneralSurgery,HospitalUniversitárioMariaAparecidaPedrossian,CampoGrande,MS,Brazil cServiceofRadiology,HospitalUniversitárioMariaAparecidaPedrossian,CampoGrande,MS,Brazil

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received28March2015

Accepted8June2015

Availableonline2October2015

Keywords:

Crohn’sdisease

Enterography Diagnosis

a

b

s

t

r

a

c

t

Proposition:Crohn’sdisease(CD)isachronicinflammatoryprocessthataffectsvariousparts

ofthegastrointestinaltract,fromthemouthtotheanuswithunknownetiologyandvariable

clinicalpresentation.CDdiagnosisisbasedonclinicalandcomplementarytests.Among

thecomplementarytests,enterographywithCTenterographyhasshowngoodresultsin

theevaluationofthisdisease.

Methods:Thepatientsevaluatedweresubmittedtoaquestionnaireontheclinical

manifes-tationsofthediseaseandanCTenterographywasobtained.Thestudieswerereviewedby

anexperiencedradiologistlookingforradiologicalsignsofCD.

Results:Themeanagewas40years,withapredominanceofwomen.Themainclinical

manifestationsarediarrheain24(70%),hematocheziain19(55%),abdominalpainin29

(85%)andweightlossin22(64%)patients.ThemainfindingsonCTenterographywerean

intestinalwallenhancementsignalin23patients(67%),vascularengorgement(vasarecta)

in20(58%),parenteralfatdensificationin14(41%),intestinalwallthickeningin22(64%),

andlymphnodeenlargementin17(50%)ofpatients.

Conclusion: ThisstudyshowedthatCTenterographypresentsagoodassessmentof

intesti-nalinvolvementbyCD.

©2015SociedadeBrasileiradeColoproctologia.PublishedbyElsevierEditoraLtda.All

rightsreserved.

Enterografia

por

tomografia

computadorizada

na

avaliac¸ão

da

doenc¸a

de

Crohn

Palavras-chave:

Doenc¸adeCrohn

Enterografia Diagnóstico

r

e

s

u

m

o

Proposic¸ão:Adoenc¸adeCrohn(DC)éumprocessoinflamatóriocrônicoqueacometevários

locaisdotratogastrointestinal,desdeabocaatéoânus,tendoetiologiadesconhecidae

apresentac¸ão clinica variável.Seu diagnósticobaseia- seno exameclinicoe em testes

Correspondingauthor.

E-mail:[email protected](C.H.M.dosSantos).

http://dx.doi.org/10.1016/j.jcol.2015.06.006

(2)

complementares.Dentreosexamescomplementares,aEnterografiaporTomografia

Com-putadorizada(Entero-TC)temmostradobonsresultadosnaavaliac¸ãodessadoenc¸a.

Metodologia: Os pacientes avaliados foram submetidos a um questionário sobre as

manifestac¸õesclinicasdadoenc¸aerealizaramEntero-TC.Essesexamesforamanalisados

porumradiologistaexperiente,àprocuradesinaisradiológicosdaDC.

Resultados: Aidade médiafoi de40 anos,compredomíniode mulheres.Asprincipais

manifestac¸õesclínicasforamdiarreiaem24(70%),hematoqueziaem19(55%),dor

abdom-inalem 29(85%)eperdadepesoem22(64%)dospacientes.Osprincipaisachadosna

Entero-TCforamosinalderealcedeparedeintestinalem23pacientes(67%),ingurgitamento

vascular(vasarecta)em20(58%),densificac¸ãodegorduraperientéricaem14(41%),

espes-samentodeparedeintestinalem22(64%)elinfonodomegaliaem17(50%)dospacientes

avaliados.

Conclusão: OpresenteestudomostrouqueaEntero-TCapresentaboaavaliac¸ãodo

acome-timentointestinalpelaDC.

©2015SociedadeBrasileiradeColoproctologia.PublicadoporElsevierEditoraLtda.

Todososdireitosreservados.

Introduction

Crohn’sdisease(CD)isachronicinflammatoryprocessthat

affects variousparts ofthe gastrointestinal tract,from the

mouthtotheanus.1,2CDhasshownanincreaseinits

preva-lence since the second half ofthe twentieth century and,

despitemajoradvancesinunderstandingthebasic

mecha-nismsofinflammationandpathogenesis,itscauseremains

unknown.1

With an extremely variable clinical presentation, CD

exhibitssymptomsandprevalentinjuriesthatdifferaccording

totheirlocation,extent,systemicmanifestationsand

poten-tialcomplications.Ingeneral,CDexhibitsasearlysymptoms:

abdominalpain,associatedwithpersistentdiarrhea,weight

loss,mildfeverandextra-intestinalmanifestations.2

The diagnosis of CD is based on the analysis of

clini-caldata,ashistoryandacompletephysicalandproctologic

examination,besidesendoscopic,radiological,laboratoryand

histologicaltests.3Undoubtedly, colonoscopyhasprovento

bethetestofchoiceforthediagnosisofthisdisease,since

itallowsacompleteevaluationofthelargebowel,ileocecal

valveandterminalileum,areascommonlyaffectedbythe

dis-ease.However,initsmostpart,thesmallintestinecannotbe

evaluatedbythismethod.

Forseveralyears,bariumstudieswereconsideredasthe

goldstandard in theinvestigation ofdiseases ofthe small

intestine,forexample,conventionalenteroclysisand

intesti-naltransit,3 withgreatimpactonthediagnosis,evaluation

oftheir anatomicaldistribution, the presenceof

complica-tionssuchasstencils,fistulae,abscesses,andsignsofacute

exacerbation.4

Withthedevelopmentofimagingstudies,the

enterogra-phy,eitherbycomputedtomographyormagneticresonance

imaging,isreplacing theintestinaltransitand enteroclysis

proceduresintheimagingevaluationofthesmallintestine.

TheadvantageofCTenterographyistoallowavisualization

oftheentiresmallintestine,withoutoverlappingloops,thus

allowing the evaluationofthe intestinal wall, detection of

extra-luminalpathological conditions,andpotential

associ-atedchanges.

Many ofthesefindingsare notseen intraditional

endo-scopicstudies,whichfavorstheprogressivereplacementof

oldmethodsbytheenterographyasthemainmethodof

diag-nosisofinflammatoryboweldisease(IBD).5–8

The early studies with CT enterography showed a high

degreeofsensitivity,above 85%,forthe diagnosis ofactive

CD,whencomparedwithbariumenteroclysis.Recentstudies

havedemonstratedasensitivityrateofupto100%and

speci-ficityof53.9%fortheidentificationofCDinitsactivephase.7

OtherpapershaveshownthatCTenterographyisequivalent

toMRenterographyfortheassessmentofCDactivity.

DespitestudiesshowinggoodresultswithCT

enterogra-phy,therearefewpublicationsonthissubjectinBrazil;thus,

itisessentialtocarryoutthisstudyinourmidst.

Goal

Theaimofthisstudywastoanalyzetheradiologicalfindings

ofCTenterography,relatingthemtotheclinical

manifesta-tionsinpatientswithCD.

Method

The study was approved by the Ethics Committee of the

Federal University of Mato Grosso do Sul. After reading

and signingan informedconsentform, patientsdiagnosed

withCrohn’sdiseasereferredfromColoproctologyOutpatient

ClinicsofHospitalUniversitárioMariaAparecidaPedrossian

and Hospital Regional de Mato Grosso do Sul were

stud-ied.

Patients diagnosed with Crohn’s disease, aged over 18

years,andalreadyevaluatedbycolonoscopywereincluded.

Patients with a known gastrointestinal tract neoplasia,

patientswithgastrointestinalsymptomssuchasnauseaand

vomiting, pregnant women, and patients with allergy to

iodinated contrast or with creatinine above 2.0mg/dl were

excludedfromthisstudy.

All participantsrespondedtoaquestionnaire(Fig.1)on

Crohn’sdisease aboutsymptomsand signs atpresentation

(3)

Fig.1–Enterographybycomputedtomographyof abdomen(sagittalsection)showingluminaldilation,wall thickeningandcontrasthyper-uptake.

Regardingthemedication used,thesedrugswere

classi-fiedasimmunosuppressants(azathioprine),salicylates(oral

mesalazine), topical salicylates (mesalazine enemas and

suppositories),corticosteroids(prednisoneandbudesonide),

biologicals (infliximab and adalimumab) and antibiotics

(metronidazoleandciprofloxacin).

An oral neutral contrast, polyethylene glycol solution

(Muvinlax®),commerciallyavailableassachetswith13.125g,

wasusedasperprotocolintheprocedures.Thisproductwas

dilutedasfollows:fivesachets(65.625g)in1500mLofwater

(43.75g/L), administered during 40min. Then, the

partici-pantsunderwentcomputedtomography(CT)oftheabdomen

andpelvis.AnAquilon-64tomographwith64rowsof

detec-tors(ToshibaMedicalSystems,Tokyo,Japan)wasused.The

examinationswereperformedwithmultislicetechniqueand

volumetricacquisition,extendingfromthediaphragmtothe

pubic symphysis, 65s after starting the intravenous

injec-tionofcontrastmedium.Thecontrastwasinjectedatarate

ofapproximately 3mL/sin aproportion of1.5mL/kg, with

a maximum volume of 150mL. The technical parameters

usedinCTscanswereasfollows:collimation64×0.625mm,

pitch=0.891,3-mmthick,120kVp,andmAs=1mm.Coronal

andsagittalreconstructionswereobtained.

Thescans were interpreted bya single radiologist with

extensiveexperience in CT enterography;this professional

wasblindedtoclinical informationathisworkstation.The

evaluatorconductedananalysisastothedegreeof

intesti-naldistension, divided into four areas ofbowel segments:

lefthypocondrium,mesogastrium,pelvisandterminalileum.

Eachregionwasratedaccordingtoascalefrom1to3,as

fol-lows:1–loops<1cmdiameter;2–loopswith1–2cmdiameter;

3–loops>2cmdiameter.Furthermore,theradiologist

classi-fiedtheloopwallsasvisibleornon-visible,alsointhefour

areasconsidered.

Thefollowingfindingsindicativeofdiseaseactivitywere

observed withCT enterography: wallthickening,increased

intestinal wall enhancement, parietal stratification,

par-enteral fat densification,vascular engorgement(vasa recta),

lymphadenomegaly,fistulaeorabscesses.

Data were analyzedusingthe ExcelWindows® program

2007.ThefindingsofCTenterographywere thencorrelated

withtheclinicalfindingsobtainedthroughthequestionnaire

onthedisease.

All informationon the identityofthe research subjects

and onquestionnairescomplied withtheethicalprinciples

ofresearchsetoutintheNationalHealthCouncilResolution

466/12.

Results

Agoodtoleranceofallpatientswithoralcontrastintakewas

noted,andalltestshavebeencompleted,totaling34studies.

Agesrangedfrom18to67years(mean,40years).Ofour34

patients,20(58%)werefemaleand14(42%)weremale.Asfor

raceorcolor,18(52%)reportedCaucasianascend,four(11%)

Black,11(32%)Brown(2%)and1Yellowpatient(Fig.2).

Themainclinicalmanifestationswerediarrheain24(70%),

hematocheziain19 (55%),abdominalpainin29(85%), and

weightlossin22(64%)patients(Fig.3).

Twenty-fivepatients(73.5%)wereunderpharmacological

treatment.Themajordrugsusedwereazathioprine(52%),oral

mesalamine(44%)andprednisone(44%),someoftheseused

incombination(Table1).Ninepatients(36%)wereusingonly

onedrug,especiallysalicylate(44%),while13(38%)wereusing

morethanonedrug(Table2).

ThemainfindingsofCTenterographywereintestinalwall

signalenhancementin23patients(67%),vascular

engorge-ment(vasarecta)in20(58%),perienteralfatdensificationin

14(41%),andbowelwallthickeningin22(64%)(Table3and

Figs.1and4).Lymphadenomegalywasobservedin17(50%)

patients.Abscesseswerealsoseeninfour(11%)patients,with

locationontheleftischioanalfossa,atthecolostomysite,right

Caucasian

Race or Color

Black

Brown

Yellow

(4)

Clinical manifestations

90%

80%

70%

60%

50%

40%

30%

20%

10%

0%

Diarrhea

HematocheziaAbdominal painWeight lossAnal fistula Fever

ConstipationArthropathy

Recurrent UTILaxative use Abdominal mass

Oral lesion

Fig.3–Signsandsymptomspresentedbyourpatientsaccordingtothequestionnaireapplied.Note:somepatients

presentedmorethanoneclinicalmanifestation.

Table1–Medicationincurrentuse.

Drug n %

Azathioprine 13 52

Mesalazinetablet 11 44

Mesalaminesuppository 2 8

Mesalazineenema 3 12

Prednisone 11 44

Adalimumab 4 16

Infliximab 4 16

Ciprofloxacin 2 8

Metronidazole 2 8

Note:somepatientsusedmorethanonemedication.

Table2–Distributionofpatientsbydrugsusedina monotherapyregimen.

Therapy n %

Immunosuppressive 2 22

Salicylate,topical 0 0

Salicylate,oral 4 44

Corticoids 2 22

Biologicals 1 11

Antibiotics 0 0

Total 9 100

Table3–RadiologicalfindingsofCTenterography.

Radiologicalsigns n %

Intestinalwallenhancement 23 67

Intestinalwallthickening 22 64

Vascularengorgement(vasarecta) 20 58

Reactivelymphnodes 17 50

Mesentericfatdensification 14 41

Stenosis 12 35

Targetordoublehalosignal 9 26

Fistulae 5 14

Abscesses 4 11

Note:somestudiespresentedmorethanonefinding.

iliacfossaandinaleftextraperitonealarea.Themostaffected bowelsegmentswereileumandrightcolon(Table4andFig.5).

Thecombinationofperianallesionsinassociationwith

uri-narytractinfectionwaspresentin10(29%)patients;two(5.8%)

weremenandeight(23%)werewomen.Diarrheaandweight

losswereobservedin19(55%)patients.

Fig.4–Enterographybycomputedtomographyofabdomen (coronalsection)showingwallthickening,luminal

(5)

Table4–IntestinalsegmentsaffectedfoundinCT enterography.

Intestinalsegment n %

Duodenum 0 0

Jejunum 0 0

Ileum 11 32

Rightcolon 9 26

Appendix 5 15

Leftcolon 6 18

Rectum 7 21

Colostomy 1 3

Note:somepatientspresentedmorethanoneaffectedsegment.

Withthedevelopmentofimagingstudies,the enterogra-phy,eitherbycomputedtomographyormagneticresonance, isreplacingintestinaltransitandenteroclysisproceduresin theevaluationofthesmallbowelbyimagingprocedures.The advantageofCTenterographyisthatthis procedureallows visualizationoftheentiresmallintestine,withoutloop over-lapping,andalsoallowstheevaluationoftheintestinalwall, detectionofextra-luminalpathologicalconditions,and poten-tialassociatedchanges.

Manyofthesefindings arenotseenintraditional endo-scopicstudies,whichsupportstheprogressivereplacementof oldmethodsbyenterographyasthemainmethodofdiagnosis forinflammatoryboweldisease(IBD).5–8

EarlystudieswithCTenterographyshowedahighdegree

ofsensitivity,above85%,forthediagnosisofactiveCD

ver-susbariumenteroclysis.Recentstudieshavedemonstrateda

Bowel wall enhancement 12

10

8

6

4

2

0

Wall thickening Perienteral fat densification Stenoses

Duodenum Jejunum Ilium

Right colon Appendix Left colon Rectum

Colostomy

Target or double halo sign Fistula

Fig.5–FindingsofCTenterography,accordingtothe affectedsegment.Note:morethanoneinthesamepatient

werefound.

sensitivityrate ofup to100%,and 53.9%specificity forthe

identification ofCD initsactivephase.7 Other publications

haveshownthatCTenterographyisequivalenttoMR

enterog-raphyintheassessmentofCDactivity.

DespitestudiesshowinggoodresultswithCT

enterogra-phy,therearefewpublicationsonthissubjectinBrazil;thus,

itiscriticalthatthisstudyiscarriedoutinourmidst.

Discussion

CTenterographyhasaclinicalapplicationintheevaluation

ofpatientswithCD,toconfirmthediagnosisofthedisease

oritsextensionandcomplicationsintheassessmentofsmall

bowel.3Nowadays,CTenterographyconstitutesanexcellent

optionforreplacementoflower-accuracyradiological

meth-odsandasanalternative versusendoscopiccapsule,avery

expensivetechnology.

Asinother studies,2 wealsoobservedpredominanceof

female patients(58%), and higherincidenceinCaucasians,

followedbyBrown,Yellow,andBlackpatients.

Inthispaper,thesectorsmostaffectedbyCDlesionswere

ileum(32%)followedbyrightcolon(26%).Iftheinvolvement

ofcecalappendix(14%)isincluded,aclearpredominanceof

involvementintheileocecaltransitionwillbenoted,

accord-ing to the literature. The large intestine was the second

mostaffectedarea,alsoaccordingtoobservationsbyother

authors.9–11

The most observed radiological signs in this study

were intestinalwallenhancementand thickening,vascular

engorgement,reactivelymphnodes,andperienteralfat

den-sification, which is inagreement with the literature,since

Costa-Silvaetal.3andIlangovanetal.12foundsimilarresults.

Considering that, at its inception, DC usually presents in

theinflammatoryform,onecanreallyexpectthatthereare

largenumbersofpatientswithwallthickeningandvascular

engorgement. Whereasmostofourpatientsevaluated had

recentdiagnoses,actuallytheseweretheexpectedfindings.

Inthisstudy,thesechangeswereobservedin88%ofpatients.

Afifietal.13alsoobservedthesekeyfindingsinpatientswith

active Crohn’s disease. Moreover, these authors compared

thesechanges versussurgical evaluationofpatients

under-going resection due to CD, and founda good clinical and

radiologicalcorrelation.

Thereseemstobenolargedifferenceinaccuracywhen

comparingCTenterographyversusMRenterography,except

that tomography is superior in detecting infectious

com-plications; and for this reason, often this technique is

recommendedasfirstchoiceintheevaluationofthe small

intestine, immediately after diagnosis, as well as in cases

wherethereissuspicionofabdominalabscesses.Inthe

fol-lowingrevaluations,maybethereisagreateradvantagewith

theuseofresonance,becausethistechniquedoesnotexpose

thepatienttoionizingradiation.Inthisstudy,wechosetouse

CTenterographybecausethisistheprocedureavailableinour

environment–afactthatisalsoobservedinmostBrazilian

medicalcenters,especiallyamongpublictertiary hospitals,

wherethereisamuchhighernumberoftomographsin

(6)

Perianal lesions associated with urinary tract infection

werepresentin10(29%)patients,two(5.8%)menandeight

(23%)women.Diarrheaandweightlosswereobservedin19

(55%)patients.Suchanassociationmayberelatedtothe

mal-absorptionsyndromeobservedinCDpatients.2

Importantly, cross-sectional studies reflect certain

momentsofthesample;thus,changesmayoccurinseveral

aspectsanalyzedover time,and withtheinclusion ofnew

patients.

Conclusion

Thestudy allowsonetoobservethatthe mainradiological

findingsofCTenterographywereintestinalwallenhancement

andthickeningandvascularengorgement,mainlyaffecting

theileumandrightcolon.Themainclinicalmanifestations

inourpatientswerediarrheaandabdominalpain.

Conflicts

of

interest

Theauthorsdeclarenoconflictsofinterest.

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1. Habr-GamaA,CerskiCTS,MoreiraJPT,CasertaNMG,Oliveira JúniorO,AraújoSEA.DiretrizesdaAssociac¸ãoMédica Brasileira.Doenc¸adeCrohnintestinal:manejo.RevAssoc MedBras.2011;57:10–3.

2. SantosSMR[TeseMestrado]Doenc¸adeCrohn:Etiopatogenia,

aspetosclínicos,diagnósticoetratamento.Porto,Portugal.:

UniversidadeFernandoPessoa;2013.Availablefrom:

http://hdl.handle.net/10284/4100

3.Costa-SilvaL,MartinsT,PassosMCF.Enterografiapor tomografiacomputadorizada:experiênciainicialnaavaliac¸ão dasdoenc¸asdointestinodelgado.RadiolBras.2010;43:303–8.

4.GlickSN.Critériosdeadequac¸ãodeexamesdeimageme radioterapia.SãoPaulo:ColégioBrasileirodeRadiologia;2005. p.309.

5.D’IppolitoG,BragaFA,ResendeMC,BretasEAS,NunesTF, RosasGQ,etal.Enterografiaportomografia

computadorizada:umaavaliac¸ãodediferentescontrastes oraisneutros.RadiolBras.2012;45:139–43.

6.HanauerSB,SandbornW.PracticeParametersCommitteeof theAmericanCollegeofGastroenterology.Managementof Crohn’sdiseaseinadults.AmJGastroenterol.2001;96:635–43.

7.CakmakciE,ErturkSM,CakmarkciS.Comparisonofthe resultsofcomputerizedtomographicanddiffusion-weighted magneticresonanceimagingtechniquesininflammatory boweldiseases.QuantImagingMedSurg.2013;3:327–33.

8.AmitaiMM,Ben-HorinS,EliakimR,KopylovU.Magnetic resonanceenterographyinCrohn’sdisease:aguideto commonimagingmanifestationsfortheIBDphysician.J Crohn’sColitis.2013;7:603–15.

9.FariaLC,FerrariMLA,CunhaAS.Aspectosclínicosdadoenc¸a deCrohnemumcentrodereferênciaparadoenc¸as

intestinais.GEDGastroenterolEndoscDig.2004;23:151–64.

10.HardtMR,KotzePG,TeixeiraFV,LudvigJC,MallutaEF, KleinubingHJr,etal.Epidemiologicalprofileof175patients withCrohn’sdiseasesubmittedtobiologicaltherapy.J Coloproct.2012;32:395–401.

11.Kleinubing-JuniorH,PinhoMSL,FerreiraLC,BachtoldGA, MerkiA.Outpatientsprofilewithinflammatorybowel disease.ABCDArqBrasCirDig.2011;24:200–3.

12.IlangovanR,BurlingD,GeorgeA,GuptaA,MarshallM,Taylor SA.CTenterography:reviewoftechniqueandpracticaltips. BrJRadiol.2012;85:876–86.

Imagem

Fig. 1 – Enterography by computed tomography of abdomen (sagittal section) showing luminal dilation, wall thickening and contrast hyper-uptake.
Table 2 – Distribution of patients by drugs used in a monotherapy regimen. Therapy n % Immunosuppressive 2 22 Salicylate, topical 0 0 Salicylate, oral 4 44 Corticoids 2 22 Biologicals 1 11 Antibiotics 0 0 Total 9 100
Fig. 5 – Findings of CT enterography, according to the affected segment. Note : more than one in the same patient were found.

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