Magnetic resonance enterography appraisal of lupus enteritis: A case report

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homepage:

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Case

Report

Magnetic

resonance

enterography

appraisal

of

lupus

enteritis:

A

case

report

Giuseppe

Cicero,

MD

∗

,

Alfredo

Blandino,

MD,

Tommaso

D’Angelo,

MD,

Antonio

Bottari,

MD,

Marco

Cavallaro,

MD,

Giorgio

Ascenti,

MD,

Silvio

Mazziotti,

MD

SectionofRadiologicalSciences,DepartmentofBiomedicalSciencesandMorphologicalandFunctionalImaging, UniversityofMessina,Policlinico“G.Martino” ViaConsolareValeria,1,Messina98100,Italy

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received27March2018 Revised8June2018 Accepted12June2018 Availableonline11July2018

Keywords:

Magneticresonanceenterography Lupusenteritis

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b

s

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Systemiclupuserythematosus(SLE)isachronicautoimmunediseasewithamultisystemic involvement.Usually,radiologicalimagingdoesnotplayacentralroleinevaluatingSLE patients,althoughitmaybehelpfulinassessingcomplications,allowingamoreaccurate evaluationofthepatient.Lupusenteritisisoneofthemostcommonandpotentiallylethal manifestationsofthegastrointestinalinvolvementofSLE.Amongtheimagingmodalities, computedtomographyscanisnowconsideredthegoldstandardinevaluatinglupus en-teritis,althoughitisimpairedbytheradiationexposure.Ontheotherhand,duringthelast decademagneticresonanceenterographyhasachievedaremarkableimportancein evalu-atingsmallbowellesionsinpatientsaffectedbyCrohn’sdisease.Wedescribethefirstcase reportoflupusenteritisevaluatedwithmagneticresonanceenterography,puttingforward theproposalofareliableandradiation-freealternativetocomputedtomographyscanin evaluatingtheintestinalinvolvementofSLE.

Introduction

Systemic lupuserythematosus (SLE) is achronic multisys-temicautoimmune disease whose specific etiology still re-mainsunknown[1,2].

Ageneticpredispositionandsomeenvironmentalrisk fac-torscontributetoitsonset,leadingtoanalteredimmune re-sponseconsistinginhyperactivationofTandBlymphocytes, lossofself-tolerance,andformationofcirculatingpathogenic

R _Competing_Interests:_None. ∗ _{Corresponding}_author.

E-mailaddress:gcicero87@gmail.com(G.Cicero).

immune complexes, withtheir consequent deposition and damageofseveralorgans[1,2].

TheoverallincidenceratesforSLEareapproximately 0.3-23.7per 100,000person-years,withaprevalencethatrange from6.5to178.0per100,000andafemale–maleratiocloseto 9:1[2,3].

Althoughthediagnosisandtheevaluationofthediseaseas awholearestrictlyclinical,theassessmentandthefollow-up ofsomecomplicationsmayrequiretheusefulnessof radio-logicalimaging.

Inparticular,thegastrointestinalinvolvementofSLEisa potentiallyseverecomplicationofSLE[4],withanincidence thatrangefrom5.4%to40%ofthepatients[5,6];amongits possible clinical manifestations, one of the most common https://doi.org/10.1016/j.radcr.2018.06.008

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islupusenteritis,animmunocomplex-mediatedvascular in-flammationthatmayleadtothenecrosisofthevesselwalls [5,7].

Accordingtothedefinitiongivenbythe BritishIsles Lu-pusAssessmentGroupdiseaseactivityindex,lupusenteritis isintendedasa“gastrointestinalSLEinvolvementaseither vasculitisorinflammationofthesmallbowel,withsupportive imagingand/orbiopsyfindings"[8].However,inliterature, lu-pusenteritisandlupusvasculitisareoftenusedassynonyms, togetherwithotherdenominations,suchasmesenteric arteri-tis,lupusarteritis,gastrointestinalvasculitis,intra-abdominal vasculitis,andacutegastrointestinalsyndrome[5,9,10].

Uptonow,allthedifferentimagingmodalitieshavenot shown pathognomonic signs related tolupus enteritis, in-cluding computed tomography (CT) scan, that is consid-eredthegoldstandardinvestigationinspiteoftheradiation exposure.

Magnetic resonance enterography (MRE) is a radiation-safe,full comprehensiveexaminationusually indicatedfor patientsaffectedbyCrohn’sdisease(CD).

However,consideringtheincreasinglyimportancethatthis techniquehas achievedduringthe last yearsin evaluating smallbowellesions,itispossibletoconsidernewfrontiersof itsperforming.

Toourknowledge,wedescribethefirstcasereportof gas-trointestinalinvolvementofSLEevaluatedwithMRE.

Case

report

Wedescribethecaseofa22-year-oldwomanaffectedbySLE whohadbeenhospitalizedtwice,in2differenthospitals,due togastrointestinalsymptoms.

Thefirsttime,anabdominalx-rayplainradiographanda CTscanwereobtained,showingsomegas–fluidlevelswithin theilealloops,whosewallswerealsothickenedandwitha layeredaspect;somecentimetriclymphnodeswerealso visi-bleinthemesentericfat,andperihepaticandperisplenicfluid collectionswereseen.

Abiopsythroughacolonoscopicexamwasalsoperformed, which showed mucosal ulcerative lesions in the terminal ileumwithcellularinfiltration andhemorrhage fociwithin theunderlyinglayersoftheintestinalwall,allowingthe di-agnosisoflupusenteritis.

Moreover, a US examination of both kidneys and an ultrasound-guidedbiopsyofthelowerpoleoftheleftkidney werealreadyperformed,demonstratingarenalhistologyof classIVlupusnephritis.

The patient was discharged after the prescription of steroidsandimmunosuppressivetherapy.

However,theimmunosuppressivetherapywaslater sus-pendedduetotheonsetofamarkedneutropenia.

After10monthsfromthelasthospitalization,thepatient cametotheEmergencyRoomofourhospitalduetothe re-crudescenceoftheabdominalsymptomsandtheoccurrence ofvasculiticurticariawithangioedemaoftherighteyeand thesuperiorlip.

Laboratory tests showed active renal disease, with in-creasedproteinuria(3040,70mg/24h),lowcomplement frac-tionC3(61,9mg/dL),lowC4(5.29mg/dL),increasedPCR(31,

54mg/L),high velocità di eritrosedimentazione(VES) value (40mm/h),positiveelevatedanti-ds-DNAantibodies(123,60 IU/mL),positiveantinuclearantibodyat1:1600,positive anti-Roantibodies,and a normallymphocyte countwith lower CD4+and/orCD8+ratio.

Inordertoassess thecurrentstatusoftheintestinal in-volvementandinaccordancewiththeclinicians,itwas de-cidedtoperformanMRE,withtheprincipalaimofsparing thepatientanotheramountofradiations.

MRE requires the oral administration of approximately 1500mL of polyethylene glycol-water solution, starting 45 minutesbeforethebeginningoftheexam.

Afterthepatientwasplacedinsupinepositioninsidethe scanner,coronalthick-sectionT2-weightedrapidacquisition withrelaxationenhancement(RARE)acquisition,axial and coronalT2-weightedtruefastimagingwithsteady-state pre-cession(repetition time/echo time: 4.20/2.10 ms, flip angle (FA):60°),andhalf-Fourieracquisitionsingle-shotturbospin echo(repetition time/echo time: ∞/80 ms) with and with-outfatsuppressionwereperformed,togetherwith diffusion-weighted imaging (DWI) sequences, obtained on the axial planeusingadiffusionfactorbfixedat0,400,and800s/mm2_.

Coronal precontrast ultrafast 3D T1-weighted gradient-echo fat-suppressed and ultrafast axial 3D T1-weighted gradient-echofat-suppressedimagesobtainedafterinjection ofgadoteratemeglumine (Dotarem)atadose of0.2mL/kg bodyweightwereacquiredat30,60,and180seconds,followed byabolusof30mLofnormalsaline.

Theexamallowedtodetectamildthickening(5mm)of severalilealloops,whosetotalextension,measuredwith dig-italcalipersfromtheileocecalvalve,amountedto38cm.

Moreover, the “thumb printing sign,” usually related to ischemic condition, was clearly detectable on T2-weighted thick-sectionRAREimages.Amoderateamountoffreefluid wasalsoseenwithintheabdominalcavity(Fig.1).

Diffusion-weighted and apparent diffusion coefficient (ADC)calculation did not show water restriction, whereas contrast-enhancedsequencesdemonstratedamild enhance-mentofthethickenedsmallbowelwalls(Fig.2).

Thepatientwastreatedwithsteroids(intravenous admin-istrationofmethylprednisolone,1g/dayfor3days)and mon-oclonalantibodies(intravenousadministrationofrituximab, 1g/day).

Afterthereliefoftheabdominalandcutaneoussymptoms andtheprescriptionofthesteroidtherapy,the patientwas discharged.

Discussion

Although several manifestations of the gastrointestinal tract involvement can be recognized in SLE patients (eg, protein-losing enteropathy, intestinal pseudo-obstruction, eosinophilicenteritis,etc.)[7],lupusenteritisremainsoneof themostcommon,affectingupto53%ofthepatients present-ingabdominalpain[4,11].

Inflammatoryenteritisisconsequenttothedepositionof circulantpathologicimmunocomplexandthrombosisofthe intestinalvessels[12];itsprevalencerangesfrom0.2%to53%

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Fig. 1 – Coronal T2-weighted half-Fourier acquisition single-shot turbo-spin-echo scan (a) showing a mild thickening of a distal ileal loop ( blackarrowheads) and free intraperitoneal fluid ( asterisk). The “thumb printing sign” ( arrows) is also easily appreciable on coronal T2-weighted thick-section RARE image (b).

Fig. 2 – Coronal T1-weighted T1 high resolution isotropic volume excitation (THRIVE) with fat saturation (FS) after Gd injection sequences (a) demonstrates mild enhancement of the small bowel thickened walls ( arrows). Axial

diffusion-weighted acquisition (b) and gray-scale ADC image (c) does not show water restriction of the same pathologic loop ( arrows). S, sigma.

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ofSLEpatients,althoughitisclinicallysignificantinonly2% ofthem[13].

Usually,themostaffectedtractofthegutistheone sup-pliedbythesuperiormesentericartery[6,14],inparticular je-junumandileum[5].

A wide spectrum of generic symptoms can be related tothiscondition,includingabdominalpain,fever,vomiting, anorexia,diarrhea,pancreatitis,besidessomecoexisting typ-icalsignsofSLE,suchasmalarrashorarthritis[12,13,15].

However,arapiddiagnosismayleadtoatimelytherapeutic approach:steroidsareusuallysufficient,otherwise immuno-suppressivetreatmentcanbechosenformoreseverecases [5].

Althoughthedefinitediagnosisandtheevaluationofthe diseaseentirelyremaininthehandsoftheclinicians, radi-ologicalimagingcanprovideausefulsupportinthe assess-mentandfollow-upofthiscomplication.

Nowadays, CT scan is considered the gold standard in imagingevaluationoflupusenteritis,allowingthedetection ofthetypicalfeaturesofischemicbowel:focalordiffusewall thickening,dilatationofthelumen,enhancementofthe mu-cosa and serosa (the so-called “target sign”),engorgement ofmesentericvessels(“thecombsign”),and mesentericfat stranding[5,6,12,13,15].Additionalreliefssuchasascites, lym-phadenopathies,andgenitourinaryinvolvementcanalsobe found[14].

Otherimagingmodalitiescanalsobeusedinthe evalua-tionofthiscondition:abdominalultrasoundcanbehelpful inrecognizingbowelsubmucosaledema,wallthickening,or ascites[11],whereasdouble-contrastradiographymayshow thickening andirregular profileoftheloop involveddueto hemorrhageandedema(the“thumbprinting” sign), suggest-ingbowelischemia[6,11,12].

However,allthoseradiologicalsignsarenotspecificof lu-pusenteritisandthedifferentialdiagnosismayinclude pan-creatitis,mechanicalbowelobstruction,peritonitis,or inflam-matoryboweldiseases(IBDs)[5].

Therefore,endoscopicandhistologicalconfirmationsare requiredinorder toget theright diagnosis andtoexclude otherconcomitantdiseases,althoughveryrare,suchasIBD [1,13].

Duringthe lastyears,MREhasalready beenincludedin theevaluationprotocolofCDpatients,duetoitsaccuracyin theappraisalofsmallbowellesionsandthelackofradiation exposureandinvasiveness[16,17].

Inthecasedescribed,thepatienthadalreadygota histo-logicaldiagnosisoflupusenteritis,whichwasassessedbyCT scanduringherprevioushospitalization.

Inordertore-evaluatetheintestinalinvolvementwiththe purposeofsparingherfromanotheramountofradiations,it wasdecidedtoperformanMRE.

Thisimagingmodalityallowedusthedetectionofsome findingsusuallyassociatedwithlupusenteritis,suchasawall thickeningofthelastilealloop,withaconcomitant inden-tationofthe mucosalandserosalsides,referabletoedema and/orhemorrhageofthesubmucosallayer,andamoderate amountoffluidcollectionwithintheabdominalcavity.

Althoughitiswellestablishedthatbothsmallbowel is-chemia and acute inflammatory conditions (eg, IBDs) are strictly related to hyperintensity on DWI and

contrast-enhancedimages,inourcasethesmallbowelwallsinvolved showedonlyamildcontrastenhancementandnosignificant waterrestriction.

The mostreasonablehypothesis thatcould explainthis scenariowouldbeafibroticprogressionofthe smallbowel wallsinvolved.AsalreadydescribedforIBDs,intestinal fibro-sisistypicallycharacterizedbyhypointensityonDWIandby adelayedhyperenhancementaftercontrastmediuminjection [18,19],whosedetectionwouldhaveneededatleastan addi-tionallateracquisition.However,beyondthesediscrepancies thatshouldbedeepenedwithfurtherstudies,inouropinion MREhasthepotentialtoplayacentralroleinevaluatingthe intestinalinvolvementofSLE.

Infact,fordifferentreasons,theimagingevaluationofthe smallbowelhasalwaysbeen problematicduetothe radia-tionexposure(CTscan),thepotentiallynonexhaustive evalu-ation(fluoroscopy),orthehealthcarecosts(videocapsule en-doscopy).

Through theingestionofthewatersolutionof polyethy-leneglycol(PEG),MREpermitstodistendtheintestinalloops, leadingtoanaccurateevaluationoftheirwall.

Themainadvantagesofthistechniqueconsistinthe com-prehensiveevaluationofthewholeabdominalcavity, includ-ingthepossibilityofdetectingextraintestinalfindings,andin itssafeness,whichconsenttoreperformtheexamaftershort periodsoftimeorevenafterfewminutes(ie,iftheintestinal loopsarenotwelldilated)[20].

Ofcourse,MREisalsoimpairedbysomelimitations,such asthescanningtime(about20-30minutes),theexpertiseof theradiologistandthecomplianceofthepatientinassuming theoralcontrastmedium.

Therefore,CTscanisstillconsideredtheimagingmodality ofchoiceinevaluationofacuteonsetofthiscondition,due toits widespreadavailability,thefasterscanningtime,and theoptimalimagequalityeveninpresenceofintraluminal gas,whichcouldindeedproducesusceptibilityartifactsonthe MREimages.

Moreover,MRE,aswellas theother imagingmodalities, couldnotestablishaconfidentidentificationoflupus enteri-tis,whichhastobediagnosedclinicallyandeventuallywith endoscopy.

However, on the basis of the lack of radiation and largeamountofinformationachievablewiththisexam,the benefits–costsratio seems toincline towardthe MRE tech-nique.

Obviously,furtherstudieshavetobeperformedinthisway toimprovethecurrentknowledgeandtoextendtheoutreach ofthistechniqueoutsidetheIBDborders.

Conclusion

Wedescribedthefirstcaseoflupusintestinalenteritis evalu-atedwithMRE,animagingmodalitynowmainlyperformedin patientsaffectedbyCD.Aswellastheotherimaging modal-ities,MREcannotallowmakingadefinitediagnosis but,in comparisonwiththem,itsuseisencouragedbysome advan-tages,suchasthelackofradiationandthehugeamountof informationachievable.

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ProbablytherealpotentialofMREinevaluatingthesmall bowelisstillnotentirelyknownandfurtherimprovementin thissensecouldbringfuturebenefitsonpatientcare,interms ofcompletenessofdiseaseassessmentandsparingof radia-tionexposure.

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