First bilateral non-invasive follicular thyroid neoplasm with papillary-like nuclear features (NIFTP) co-occurring with bilateral papillary thyroid microcarcinoma: Case report and literature review

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ContentslistsavailableatScienceDirect

International

Journal

of

Surgery

Case

Reports

j o ur na l h o m e p a g e :w w w . c a s e r e p o r t s . c o m

First

bilateral

non-invasive

follicular

thyroid

neoplasm

with

papillary-like

nuclear

features

(NIFTP)

co-occurring

with

bilateral

papillary

thyroid

microcarcinoma.

Case

report

and

literature

review

Mohamed

S.

Al

Hassan

_,

_Walid

_El

_Ansari

_,

_Abdallah

_Elshafeey

_,

_Mahir

_Petkar

_,

Abdelrahman

Abdelaal

a_{DepartmentofGeneralSurgery,HamadGeneralHospital,Doha,Qatar} b_{DepartmentofSurgery,HamadGeneralHospital,Doha,Qatar} c_{CollegeofMedicine,QatarUniversity,Doha,Qatar}

d_{SchoolofHealthandEducation,UniversityofSkövde,Skövde,Sweden} e_{WeillCornellMedicine–Qatar,Doha,Qatar}

f_{DepartmentofLaboratoryMedicine&Pathology,HamadGeneralHospital,Doha,Qatar}

a

r

t

i

c

l

e

i

n

f

o

Received28November2020 Accepted30November2020 Availableonline2December2020 Keywords:

NIFTP Casereport Thyroidnodule Management

Papillarythyroidmicrocarcinoma Bilateral

a

b

s

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INTRODUCTION:Non-invasivefollicularthyroidneoplasmwithpapillary-likefeatures(NIFTP)isarecently characterizedlesionwithverylowmalignantpotential.Thishasallowedforlessaggressivemanagement ofthistumorsubtype.Papillarythyroidcarcinoma(PTC)hasmalignantpotentialandrequiresdifferent considerationsinmanagement.

PRESENTATIONOFCASE:A33-year-oldwomanpresentedtoourThyroidSurgeryClinicwithaleftneck swellingslowlyenlargingover4years,andrecentright-sidedneckpain.Neckultrasoundandfineneedle aspirationforcytologyfoundbilateralthyroidnodules,labelledas‘follicularlesionofundetermined significance’(FLUS).Finalpathologyreportaftertotalthyroidectomyidentifiedfourdistincttumors: bilateralNIFTPlesionsandbilateralpapillarymicrocarcinomas.

DISCUSSION:ManagementofNIFTPcomprisespartialortotalthyroidectomywithoutfurther interven-tion.ManagementofPTCisthesamebutwiththepossibleadditionofradioactive ablationdueto theincreasedmalignantpotential.ThisisthefirstreportofbilateralNIFTPlesionsandbilateral pap-illarymicrocarcinomasco-occurringtogetherinthesamepatient,somanagementwaschallenging.The decisionwasmadetogivethepatientlowdoseradioactiveiodineablationandcontinuemonitoring. Ultrasoundoftheneckfollowup6monthslatershowednoresidualthyroidtissueorlocalrecurrence. CONCLUSION:Althoughrare,NIFTPcanco-occurwithPTC.BilateralNIFTPwithbilateralPTCisextremely rare.Surgeonsandpathologistsneedtobeawareofthisrareentitythatcanco-occurinboththyroid lobes.Totalthyroidectomyisthedefinitivetreatment.Post-surgerysurveillanceisimportantandfollow upneedstobewatchfulforanyrecurrenceormetastasis.

©2020TheAuthor(s).PublishedbyElsevierLtdonbehalfofIJSPublishingGroupLtd.Thisisanopen accessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/).

1. Introduction

Thyroid canceris anincreasingly important due tothe dra-maticincreaseindiagnosedcasesduringthelast30years[1].Even thoughthe5-yearsurvivalrateis97.8%[1],thyroidcancerhas significantimpact,whereintheUSAalone,$1.6billionhasbeen spentonthemanagementofthyroidcancerduring1985–2014[2]. Extensiveeffortshavebeenmadetoappropriatelyclassifythyroid tumorsbasedontheirpotentialformalignancyinorderto man-agebenignlesionslessaggressively.In2017,theWHOreleaseda

∗ Correspondingauthorat:DepartmentofSurgery,HamadGeneralHospital,Doha, Qatar.

E-mailaddress:welansari9@gmail.com(W.ElAnsari).

newclassificationforthyroidtumorstofurtherclassifypreviously misunderstoodlesions[3].

Mostwelldifferentiatedthyroidtumorscanbeclassifiedinto thebroadfollicularandpapillarycategoriesbasedonthe histo-logicalcharacteristics.Folliculartumors(10–15%prevalenceofall thyroidcancers)comprisefollicularcellslinedbycuboidal epithe-liumandarefurthercharacterizedbasedontheirinvasivebehavior [4,5].Folliculartumorsthatdonotinvadethecapsulearefollicular adenomas,andthosethatshowevidenceofinvasionarefollicular carcinomas[4].Papillarythyroidcancer(PTC,themostcommon typeofthyroidtumors)isanepithelialtypetumor,carriesthebest prognosis,andisdifferentiatedfromthefollicularsubtypebyits uniquenuclearfeatures[5].

A very unique and recently characterized thyroid lesion is thenon-invasivefollicular thyroidneoplasmwithpapillary-like

https://doi.org/10.1016/j.ijscr.2020.11.159

2210-2612/©2020TheAuthor(s).PublishedbyElsevierLtdonbehalfofIJSPublishingGroupLtd.ThisisanopenaccessarticleundertheCCBY-NC-NDlicense(http:// creativecommons.org/licenses/by-nc-nd/4.0/).

Fig.1. USoftheleftthyroidnodule.

features(NIFTP).Thistypehasdistincthistopathologicaland clin-icalcharacteristics.Formerlyknownasnoninvasiveencapsulated follicularvariantofpapillarythyroidcarcinoma,NIFTPbehaves dif-ferentlyfromtheclassicPTC.Mostimportantly,NIFTPhasavery indolentcourseandrarelyexhibitsmalignantpotential[6],making itimportanttodistinguishfromothermoremalignanttumors.A studyof108patientsshowedthatNIFTPexhibitednorecurrence 1–10yearsaftersimplelobectomy[7].DiagnosisofNIFTPismade aftercompleteresectionandconfirmationofcriteriasuchasthefull encapsulationofthetumor,nuclearfeatureofPTC,follicularpattern ofgrowthwithnopsammomabodies,nocapsularorvascular inva-sion,andnoevidenceofnecrosis[7].Moleculartestingisamajor partofthediagnosisduetotheuniquegeneticmakeupofNIFTP thatincludesmarkerslikeanactivatingmutationinoneoftheRAS genes(NRASmostcommon,36–67%),PAX8-PARGrearrangement (4–22%),andTHADAfusions(22%)[8]

Wepresentapatientwithaleftsidedneckswellingthat,after totalthyroidectomy,wasfoundtohavebilateralNIFTPsinaddition tobilateralpapillarythyroidmicrocarcinoma.Tothebestofour knowledge,thisisthefirstcasereportofthisnature.Wereport thiscaseinlinewiththeupdatedconsensus-basedsurgicalcase report(SCARE)guidelines[9].

2. Casepresentation

A33-year-oldEgyptianfemalepatientpresentedatourThyroid SurgeryOutpatientClinicatHamadGeneralHospitalinDoha,Qatar witha4-yearhistoryofleftneckswelling.Shealsocomplainedof arecentfeelingofsomediscomfortandneckpainontherightside, butnochangeofvoice.Herpastmedical,socialandfamilyhistory wereunremarkable.Shehadnohistoryofchronicmedical condi-tionsandheronlysurgicalhistorywasalowersegmentcesarian sectionafewmonthsbeforehercurrentindexpresentation.She didnotsmoke,neverconsumedalcoholandwasnotonlong-term medications.Therewasnofamilyhistoryofthyroidcancer,and nopasthistoryofneckirradiation.Physicalexaminationrevealed aleftthyroidlobeenlargement,about3×3cm,thatmovedwith swallowing.Therightthyroidlobewasnotpalpable.Therestof thephysicalexaminationwasunremarkable.

BloodworkuponpresentationshowednormalTSHandfreeT3 andT4.Intialultrasound(US)ofthethyroidglandatasecondary hospitalshowedenlargementoftheleftlobe(5.3×2.2×3.5cm),as wellasacomplexnodule(4.2×1.8×2.2cm)thatoccupiedmostof theleftlobe,containingacystwithathickirregularwallandclear contents withperipheralvascularityandnointernalvascularity. Bothsubmandibularandparotidglandswereunremarkable,and therewasnocervicallymphadenopathy.

Fig.2. LeftlobeNIFTPwithwellcircumscribedandthincapsule.HandEx2.

ShewasreferredtoourThyroidSurgeryOutpatientClinicat thetertiaryhospitalforUSguidedfine-needleaspirationfor cytol-ogy(FNAC)(Fig.1).WeundertookFNACbiopsyofthis leftlobe nodule.DuringtheFNACprocedure,theUSshowedanothersolid noduleintherightlobethatwasalsoaspirated.Theaspiratefrom bothnodulesshowedhighcellularitycomprisedoffollicularcells arrangedin analteredarchitectural background,suggestingthe histopathologicdiagnosisofthetwonodulesas‘follicularlesionof undeterminedsignificance’(FLUS).Thecasewasdiscussedatour thyroidmulti-disciplinarymeeting(MDT)andthedecisionwasto undertaketotalthyroidectomy.Thesurgerywasundertakenbyan experiencedthyroidsurgeonandwasuneventful.

The thyroidectomy specimen weighed 23 gm. The right lobemeasured4×1.5×1.5cm, whereas theleftlobemeasured 5×2.5×2.5cm.Therewasawelldemarcatednoduleintheright lobemeasuring1.3cminmaximumdimensionandasimilar,but larger,thinlyencapsulatednodule,measuring3cminmaximum dimension,intheleftlobe.Microscopically,bothnodulesdisplayed featuresofNIFTP.Theneoplasmshadafolliculararchitecturewith lesionalcellsexhibitingnuclearclearingandprominentgrooves. HBME1immunostainwasstrongly anddiffusely positive, while stainingforBRafV600Ewasnegative.Inaddition,thereweretwo separatefociofpapillarymicrocarcinoma,locatedintherightand leftlobes,measuring0.8cmand0.3cmrespectively, demonstrat-ingtypicalnuclearcharacteristics(nuclear clearing,overlapping andgrooves)withareasofpapillarymorphology.Background lym-phocytic thyroiditisand adenomatoidnodules were also noted (Figs.2–6).

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M.S.AlHassanetal. InternationalJournalofSurgeryCaseReports78(2021)411–416

Fig.3.RightlobeNIFTPwithcharacteristicwellcircumscribedarchitecture.Hand Ex2.

Fig.4.Papillarymicrocarcinomawithtumorcellsshowingtypicalnuclearfeatures includingoverlapping,clearingandgrooves.HandEx20.

Fig.5.NIFTPdemonstratingstrongHBME1staining.

Twoweeksafterthesurgery,non-stimulatedthyroglobulin(TG) was <0.1ng/mL, and TGantibodies waspositive (133.5 IU/mL). Hence,MDT recommendedlow-doseradioactiveiodinetherapy (oralintakeof869MBqofradioactiveI-131capsule),followedby wholebodyscanwhichshowedasmallamountofactivityinthe thyroid bed.Therewasnoevidenceofdistantabnormaluptake (Fig.7). Threemonthslater, theblood test showed TGlevel of 0.1ng/mL,andtheTGantibodiesexhibitedadropfrom133IU/mL

Fig.6. NegativeBrafV600EimmunostainintheNIFTP.

to36.9IU/mL.Thepatientwasputonsuppressivelevothyroxine therapy,andscheduledforfollowupevery6monthsbyUSofthe neck,andthyroglobulintumormarkers.Themostrecentfollowup US6monthslatershowednodefiniteresidualthyroidtissueor localrecurrence.

3. Discussion

Tothebestof ourknowledge,this is thefirstreportedcase ofbilateralNIFTPswithsimultaneousbilateralpapillarythyroid microcarcinoma.Hence,wewereunabletofindothersimilar pub-lishedcaseswithwhichwecandirectlycompareourfindingswith. Weprovidealiteraturereviewofthe4publishedcasereportsof NIFTP.DespitethataremanycasesofNIFTPreportedinliterature aspartofbiggertrialsorsystematicreviewoftrials,wereportthese 4casesalongwithours,duetotheuniquefeaturesofeachofthem. Oneofthecasesoccurredina10-year-oldchild,twocaseshad spin-dlecellmetaplasiawithinthelesion,andlastly,oneofthelesions occurredwithinaHurthlecelladenoma(Table1).

Todate,therehavebeen1430reportedcasesofunilateralNIFTP [7],buttothebestofourknowledge,noreportsofbilateralNIFTP.In addition,noneofthese1430reportedcaseshadassociated micro-carcinoma,and none had bilateralassociated microcarcinomas. Hencethecurrentcaseisveryuniqueandpresentssomechallenges inthemanagementthathavenotbeendescribedbefore.

NIFTPhasbeenrecentlycharacterizedasathyroidtumorthat exhibitsanindolentbehavior.Such characterizationallows clin-iciansto approach NIFTP in a less aggressive way than before, limitingtheneedforextensivetherapyandunnecessarysideeffects associated with aggressive measures [6]. A recent review that examined11NIFTPstudieswithlargepatientpopulationsobserved nodeathsduetoNIFTPandonly1caseofpulmonarymetastasis[7]. Giventhemortalityandmetastaticevidencethatthisreview pro-vided,theparadigmformanagementofNIFTPshiftedconsiderably andnowcentersaroundsimplelobectomyfortheNIFTPinsteadof addingradioactiveiodineaswell[6].

Intermsofpresentation,ourreviewoftheliterature(Table1) shows that mostNIFTP casespresented asymptomatically with eitherafullyenlargedthyroidorenlargementofasinglelobe.We areinagreement,ourpatientpresentedwithleftthyroid enlarge-mentwhichcanbeconsideredaclassicalpresentationofthyroid nodules.However,thetablealsoshowsthatonepatienthadan unusualpresentation[10],withupperextremitynumbnesswhich isnotnormallyasymptomofthyroidnodulesunlesstheyinvolve theparathyroidglandand influencecalciumhomeostasis. How-ever,ourpatientalsocomplainedofrecentrightsidedneckpain.

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Abdou[12]Egypt2020 10 F UnilateralRt Enlarged thyroid observedby mother TwoNIFTP lesionsonR side

N Euthyroid Twosuspicious

nodulesonRt side Sheetsof follicular epithelialcells Total thyroidectomy No 12m,noRor Mt

Pigac[16]Croatia2018 42 F b _Slightly

enlarged tenderthyroid NIFTPlesion withina Hurthlecell adenoma

N Euthyroid Enlargedboth

lobes, hypoechoic structureinRt lobe

Hurthlecells Rt

hemithy-roidectomy switchedto total thyroidectomy

No N

AlRasheed[10]USA2017 76 F a Upper

extremity numbness. Multinodular goiter NIFTPwith spindlecell metaplasia N Euthyroid Multinodular goiter, Dominant noduleinRt upperpole.No microcalcifica-tions Follicularand Hurthlecells Total thyroidectomy No 2mnoRorMt

Arnoux[11]Switzerland2017 37 F UnilateralL Largenodulein

Lthyroid enlargingsince 2005 NIFTPwith focalspindle cellmetaplasia N Euthyroid Isoechogenic noduleinL thyroidlobe FNA12years earliershowed benignfindings L lobo-isthmectomy No N

Duetospacelimitations,onlythefirstauthoriscited;a_{Patienthadmultiplenodulesthroughoutthethyroid,butthecasereportonlycommentedontheNIFTPlesion;}b_{Onultrasoundtwolesionswerefound,oneontheright} andoneontheleftbutthecasereportdidnotcommentontheleft-sidedlesion;FNAC:FineNeedleAspirationforCytology;G:Gender;L:Left;Mt:metastasis;m:months;N:no;NIFTP:non-invasivefollicularthyroidneoplasm withpapillary-likefeatures;R:recurrence;Rt:Right;TFT:ThyroidFunctionTests.

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Fig.7.Postlow-doseradioactiveiodinetherapywholebodyscanshowingsmallamountofactivityinthethyroidbed.

Asregardstothyroidinvolvement,Table1depictssome varia-tionintermsoftheextentoftheinvolvementofthethyroid.While onecasehadmultinodularenlargementofthegland[10],others [11,12]presentedwithenlargementofonlyonehalfofthegland. Givensuchanextentofvariation,thereseemstobenofixedsetof physicalexaminationfindingsorpresentationthatcanprovidean indicationtothesurgicalteamastonatureofthelesions.

In terms of investigations, thyroid function tests (TFTs) are required todeterminetheactivityofthethyroidgland.Table1 showsthatinallthecasesreviewed,thepatientswereeuthyroid indicatingthatthenoduleswerenotactive[10–12,16].Wearein agreement, ourpatientwaseuthyroid,althoughthepatienthad deliveredaroundonemonthbeforethefirstsetofTFTswhichcould causeunexpectedendocrinefluctuations.Suchfluctuationshave beenshowntooccurinaround5%ofwomenfollowingdelivery [13].

Asfor imaging,Table1 depictsthat theUSfindings differed considerablybetweencasesthatourreviewidentified.The pub-lished caseswereviewedexhibitedvariableechogenicityonUS scan. Suchhypoechoic,hyperechoicorisoechogenicUS findings [11,14,16]aresupportedbyothers whodescribedNIFTPlesions aswell-circumscribedwithwidelyvariableechogenicity[14].In addition,initialUSonlyshowedtheleftsidedcomplexcystic nod-ule;onlyonUSguidedFNAwasthesecondnoduleontheright sideidentifiedandaspirated.USfindingsareoperatordependent, andtherecouldbesomelimitationsofUSwhenemployedforthe assessmentofthyroidnodules,wherenodulesthataretoosmall mightnotbeidentifiedwithgreataccuracy.HenceUSfindingsof thethyroidshouldbeinterpretedwithcautionbecauseitdoesnot haveperfectsensitivity[15].

AsfortheUSguidedFNAC,Table1showsthatallthecasesthat ourreviewidentifiedexhibitedfollicularcellsinabackgroundof colloidorbenigncells.SomeofthestudiesalsofoundHurthlecells [10,16].Inourcase,FNACofbothrightandleftnodulesshowedan abundanceoffollicularcellsinanalteredarchitecturesuggesting FLUS.AlimitationofFNACisthatitdoesnotprovideinformation regardinginvasionofthecapsulewhichisessentialinthediagnosis ofNIFTP[6].

Intermsofmanagement,basedonourcombinedUSandFNAC results,afterMDTmeeting,thedecisionwastoundertaketotal thy-roidectomy.Thiswasundertakenbyanexperiencedsurgeon.The finalhistopathologicexaminationfoundthatthetwomasses iden-tifiedonimagingwerebothNIFTP,andalsoreportedtwoadditional smallmassesofpapillarymicrocarcinomas.

Such presence of four separate tumors presented a huge dilemmatotheteamastothebestwayforwardwiththispatient’s management.Ontheonehand,NIFTPisestablishedasarelatively benignlesionwithalmostnochanceofrecurrenceafterresection. Table1showsthatalltheNIFTPcasesthatourreviewidentified weremanagedbysimpleresectionoftheinvolvedthyroidgland andsubsequentfollowup.Ontheotherhand,contrarytoallthe othercasesinTable1,ourpatienthadtwoNIFTPsandtwo papil-larymicrocarcinomas.Inaddition,thepatienthadelevatedtumor markerthyroglobulinsuggestingsomemalignantpotential, prob-ablyof the papillarymicrocarcinomas.The decision, after MDT meeting,wastogivethepatientlowdoseradioactiveiodine abla-tion,bothasadiagnosticmeasure(toidentifyanyresidualthyroid tissue)andalsotherapeutic.

In terms of recurrence and metastasis, US follow up of our patientat6monthsshowednoevidenceofeither.Thepatient, how-ever,remainsbeingmonitoredevery6monthsinordertoassess

notexcludetheco-occurrenceofotherpapillarymicrocarcinomas lesions. Conflictsofinterest Nothingtodeclare. Sourcesoffunding Nothingtodeclare. Ethicalapproval

ApprovedbyMedicalResearchCenter,HamadMedical Corpo-rationreferencenumber(MRC-04-20-1090).

Consent

Writteninformedconsentwasobtainedfromthepatientfor publicationofthiscasereportandaccompanyingimages.Acopy ofthewrittenconsentisavailableforreviewbytheEditor-in-Chief ofthisjournalonrequest.

Authorcontribution

Mohamed S. Al Hassan: Conceptualization, Data curation,

Investigation,Writing -review &editing. WalidElAnsari: Con-ceptualization,Datacuration,Investigation,Methodology,Project administration,Writing-originaldraft,Writing-review&editing.

Abdallah Elshafeey: Data curation,Investigation, Methodology,

Writing-originaldraft,Writing-review&editing.MahirPetkar:

Laboratorydata,Writing-review&editing.Abdelrahman

Abde-laal:Datacuration,Writing-review&editing.

Allauthorscriticallyreviewed,revisedandcontributedtothe finalarticle.Allauthorsreadandapprovedthefinalmanuscript.

Registrationofresearchstudies

researchregistry6272 available at: https://www. researchregistry.com/browse-the-registry#home/

registrationdetails/5fba4ae0d3b0b1001e41b262/.

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