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| | Received:6October2016 Revised:7March2017 Accepted:8March2017 DOI: 10.1111/myc.12622 ORIGINAL ARTICLE Oral paracoccidioidomycosis: Retrospective analysis of 55 Brazilian patients Aline Heloísa Trindade1 | Henrique Côrtes Meira1 2 César Tanos de Lacerda 1 DepartmentofClinicalPathologyand Surgery,SchoolofDentistry,Federal UniversityofMinasGerais,BeloHorizonte, MG,Brazil 2 DepartmentofDentistry,Universitycenter NewtonPaiva,BeloHorizonte,MG,Brazil Correspondence Dr.VagnerR.SantosPhD,Faculdadede OdontologiaUFMG,BeloHorizonte, MG,Brazil. Email:[email protected] Funding information None. | Igor Figueiredo Pereira1 | Ricardo Alves de Mesquita 1 | Julio | Vagner Rodrigues Santos1 Summary Paracoccidioidomycosis(PCM)isararefungalinfectionintheworld,butendemicand acquiredexclusivelyinLatinAmerica,withthehighestprevalenceinSouthAmerica and Brazil, particularly. Changes in oral cavity are common and constitute the first clinicalmanifestationinmanypatients.TheaimofthisstudywastodescribetheprevalenceoforalPCMandanalysetheprofileofthediseaseandpatients.Retrospective research,consistingofinformationpresentinthemedicalrecordsintheperiod19982015, whose histopathological diagnosis was oral PCM. Fifty-five oral PCM cases were confirmed. Of these patients, 90.9% were males and 9.1% were females. The average age was 49.66years and the most reported occupation was rural workers. Thepainfulsymptomatologywaspresentin61.82%ofpatients.Erythematouslesions werepredominantin73%ofthem.Insinglelesions(22cases),themostcommonlocationswerejugalmucosaandtongue.Inmultipleinvolvement(30cases),themostaffectedregionswerelips,jugalmucosaandalveolarridge.EpidemiologyofPCM,was similartoseveralotherstudies,especiallyinBrazil.Thisisthemostimportantfungal infectioninLatinAmericaandtherecognitionoforallesionsisextremelyimportant,as isoftenthefirstandinmanycasestheonlymanifestationofthedisease. KEYWORDS Brazilianpatients,epidemiology,oralparacoccidioidomycosis,retrospectivestudy 1 | INTRO DUCT IO N form,responsiblefor10%ofpatients,ischaracterisedbyanabruptand severeprogressionofinfectionthataffectschildrenandyoungpeople Paracoccidioidomycosis(PCM)orSouthAmericanblastomycosisisa ofbothsexes.Thechronicform,whichisseenin90%ofcases,affects deepfungalinfectioncausedbythedimorphicfungusParacoccidioides adults,mostlymaleandpresentswithprimarypulmonaryimpairment brasiliensis.1,2 It is a rare disease in the world, but endemic and ac- and,secondary,mucosallesions,skin,lymphnodesandadrenalglands.6 quired exclusively in Latin America, with the highest prevalence in SouthAmericaandBrazil,particularly.3 Changesintheoralregionarequitecommonandconstitutethefirst clinicalmanifestationinmanypatients.Theyarevirtuallypathognomonic Thismycosispredominantlyaffectsmiddle-agedmale,engagedin anddescribedasmoriformlesions:granular,erythematousorulcerated ruralactivities.4Theincidenceishigherintypicallyhumidgeographic appearancecontouringbyjaggededgeswithathinhaemorrhagicdot- areas,withrainfallhighlevelsandacidicsoils.1Accordingtoepidemi- ted.Theyarelocatedinvariousplaces:lips,gingiva,tongue,mouthfloor, ologicalstudiesconductedinLatinAmerica,around50%oftheinhab- buccalmucosa,uvula,pharynxandcervical-facialregions.7,8 itantsofendemicareashavebeenexposedtothefungus,butasmall proportionofpatientsdevelopaclinicalmanifestation.5 Thetreatmentcomprisesadditionofantifungalagentsandtheuse of measures to improve the general condition of the patient. Some Clinically, PCM presents two distinct patterns, according the in- controlledstudiesandcaseserieshaveshownthatazolesfastaction cubationperiodandtheprofileoftheaffectedindividuals.Theacute andsulfaderivativesareusefultherapeuticoptionsformilderformsof Mycoses. 2017;1–5. wileyonlinelibrary.com/journal/myc © 2017 Blackwell Verlag GmbH | 1 | TRINDADE ET Al. 2 thediseasewhileinmoderate/severecases,longertreatmentsorparenterallyareneeded,especiallywhenthereismucosalinvolvement.9 TheepidemiologicalapproachtoPCMisdifficult,sinceitsnotifica- T A B L E 1 Frequency,clinicalcharacteristicsandmeansofremoval oflesionsofparacoccidioidomycosispresentintheoralcavityof patientsattendedattheFacultyofDentistryofUFMG tionisnotcompulsory.Theprevalencecalculations,incidenceandmorbidityarebasedonreportsofepidemiologicalstudiesandcaseseries.10 The aim of this studywas to assess the prevalence of oral PCM and analyse the profile of the disease and patients diagnosed at Frequency Variable N % Manifestation Maxillofacial Pathology Laboratory of the School of Dentistry in the Primarylesion 46 83.64 FederalUniversityofMinasGerais,Brazil. Recurrentlesion 1 1.81 Not determined 8 14.55 Present 34 61.82 Absent 13 23.63 8 14.55 Incisionalbiopsy 47 85.45 Excisionalbiopsy 03 5.45 Not determined 5 9.10 Painfulsymptomatology 2 | M AT ERIALS AND MET HO DS Thisisaretrospectiveandobservationalstudy.Thesampleconsisted of information present in medical records of patients diagnosed whit oral paracoccidioidomycosis (PCM) in Laboratory of Oral and MaxillofacialPathologyoftheFacultyofDentistry,FederalUniversity ofMinasGerais,BeloHorizonte,Brazil,intheperiod1998-2015(18 years).Thereferredlaboratoryisanimportantdiagnosticcenterand meets the demand for histopathological examinations of the public andprivateservices,beingareferenceinthearea. Not determined Diagnosistests Colourationsofthelesions Erythematous 40 73 Thefollowingvariablesrelatedtopatientswerecollected:gender, age, profession and skin colour. Regarding infection, the data were gathered about their location, colour, symptoms, early or recurrent signsandfinaldiagnosismethods. DatawereenteredandtabulatedusingSPSS(StatisticalPackage for Social Sciences), version 22.0, which were statistically evaluated andconvertedtopercentages,tablesandgraphs.Thisstudywasapproved by the Ethics Committee of the School of Dentistry, Federal UniversityofMinasGerais(No.51017615.7.0000.5149). 3 | RESULTS FromJanuary1998toDecember2015,55oralPCMtotalcaseswere confirmed. Of these patients, 50 (90.9%) were males and 05 (9.1%) were females, with a ratio of 10:1 (Figure.1). The average age was 49.66years,range06-81years.Inaddition,thedistributionforskin colour were as follows: Afrocaucasian 22 (40.0%), Caucasian 15 (27.27%)andblack12(21.82%).Theseskincolourdatawereabsents in6charts(10.90%). Among the chips with information available, the most reported occupation was agricultural/rural workers (11 cases), followed by F I G U R E 1 Distributionofpatientswithoralparacoccidioidomycosis (PCM)accordingtogender constructionworker/builder(6cases).Another14caseswerevarious otherprofessionssuchassurveyor,carpenterandtrader. F I G U R E 2 Histologicaspectoffungal structuresofParacoccidioides brasiliensis, indicatedbythearrows:(A)Haematoxylin andeosinstaining,(B)Grocott-Gomori staining(40X) | 3 TRINDADE ET Al. T A B L E 2 OralParacoccidioidomycosis(PCM)lesionsdistribution accordingtotheirlocation sites.Itisobservedthatinindividualswhohadsinglelesions,themost commonlocationswerejugalmucosaandtongue.Alreadyinmultiple involvement, the most affected regionswere lips, jugal mucosa and Injuries location N % alveolar ridge. Figures3A,B,C shows the multiple oral manifestation Single N % Multiple Mouthfloor 0 0,00 Mouthfloor 6 7,69 Lipcommissure 1 4,55 Lipcommissure 3 3,85 Lobbyfund 1 4,55 Lobbyfund 2 2,56 Gingiva 2 9,09 Gingiva 5 6,41 Lip 2 9,09 Lip 15 19,23 Tongue 3 13,64 Tongue 3 3,85 Buccalmucosa 2 9,09 Buccalmucosal 5 6,41 Jugalmucosa 7 31,82 Jugalmucosa 11 14,10 Oropharynx 0 0,00 Oropharynx 5 6,41 Hardpalate 2 9,09 Hardpalate 7 8,97 Softpalate 1 4,55 Softpalate 6 7,69 ease.Notificationisnotalwaysmandatory;asignificantproportionof Alveolarridge 1 4,55 Alveolarridge 10 12,82 infected patients do not have clinical repercussions and many cases ofparacoccidioidomycosisinthegingiva,palateandoropharynx. 4 | DISCUSSION EventhoughthisstudyisshowingtheepidemiologicalaspectsofparococcidioidomycosisinBrazil,itisimportanttorememberthatsome casesofthediseasehavealreadybeendiagnosedinothercountries, suchasSpain,12Japan,13Austria,14andGermany,15.Althoughthisdiseaseisnotendemicinthosecountries,thesediagnosesmayberelated tothefarmerortouristswhoweretravelinginBrazilorCentralAmerica. Thereisadifficultyindeterminingtheactualfrequencyofthedis- goundiagnosedbecauseoflackofknowledgeofhealthprofessionals, The used test for lesions diagnosis was incisional biopsy in 47 (85.45%) cases and excision in 03 (5.45%) of them. In five records, lackofpatientsaccessanddisabilitylaboratorydiagnosisinsomeendemicareas.10 this information was not present. Figure2A,B shows two histologi- AccordingtoMartinez,3over15000casesofPCMwerereported cal staining methods used by service: haematoxylin–eosin (HE) and in LatinAmerica between theyears 1930 and 2012 and more than Grocott-Gomori (silver impregnation).Table1 shows the clinical fea- 12000casesinBrazil.Theirstudy,basedonlargedataseriesofcases turesfindingsofthe55patientswithPMClesions. shows a high annual average number of cases reported in Brazil in In 46 cases (83.64%) the disease had a primary manifestation; endemic areas: southeast, south, central west and currently in the Therewasonlyonecase(1.81%)ofrecurrentmanifestation,whereas westernAmazonregion.TheirincidenceinColombia,Venezuelaand in eight charts therewas no indication of the type of manifestation Ecuador, with an annual number of cases, is much smaller than in of paracocidioidomycosis:whether primary or recurrent.The painful Brazil. symptomatology was present in 34 patients (61.82%), 13 (23.63%) Itisadiseasethatcanbefatalandwhichmanifestsitselfwitha wasabsentandwasnotdeterminedineight(14.55%).Erythematous wide spectrum of clinical presentations, including frequent oral le- lesions were predominant in 40 (73%) of the subjects, followed by sions.2Theoralmucosamanifestationsoftenrepresentthemainclin- whitecolour(7,27%).Normalmucosal-likecolourwasobservedin4 icalsignrepresentingrepresentativenumbersbetween39.38%16 and patients (7,27%). On the other hand, 3 patients (6%) of the lesions 50%ofpatients.17 presentedmixedcoloration,beitamixtureofyellow,redandwhite. Thisstudyisananalysisof55patientswithoralPCMinaperiod Therewasnoinformationaboutthecolourlesionsin4charts(7,27%). of18years.Allcaseswerediagnosedbyasinglelaboratory,located Ofthe52caseswithavailableinformationastotheirlocationand in the capital of Minas Gerais,which geographically is located in an scope,30ofthemweremultipleinjuriesand22hadlesionsinonly endemicregioninBrazil.Mostaffectedindividualsweremen(90.9%), one location. Table2 shows the lesions distribution in the affected inthefourthdecadeoflifeandpredominantlyAfrocaucasian(40%). F I G U R E 3 Clinicalaspectoforalparacoccidioidomycosis(PCM)atmultiplesitesinthesamepatient:(A)Gingiva,(B)Palate,(C)Oropharynx. Notethemoriformappearance:granularanderythematous,contouredbyjaggededges. | TRINDADE ET Al. 4 Paracoccidioidomycosisprevailsamongmen,butthemale:female orallesions.Theincisionalbiopsywasthemostusedtechnique(85.45% ratio varies according to geographical region. In the Southeast and ofcases)fordiagnosis,andshowntobeeffectiveinthediagnosisof MidwestBrazil,itrangesfrom3:1to10:1,reachinggreaterproportions, orallesionsasdemonstratedinotherstudies.4,6,19,20Somedifferential closeto100:1innumberofcasesofsouthernBrazilandotherSouth diagnosisshouldbeincludedtosuchinjuries,especiallysquamouscell 3 Americancountries. Thisstudyevaluatedthemanifestationoforalle- carcinoma,tuberculosis,sarcoidosisandWegener’sgranulomatosis.1 sionsandmanrelationship:foundthatwomenwere10:1,similartopre- Regardingthelocationoftheorallesionsof52caseswithavailable viouswork.4,10,18-20Bicalhoetal.1foundanevenhigherproportionof information,30ofthemweremultipleinjuriesand22hadlesionsin maleinvolvement(30:1)thatthisworkandstressedthatalthoughmen only one location. Multiple injuries affected predominantly the lips, andwomenarealsoinfectedwithP. brasiliensis,womenareprotected oralmucosaandalveolarridge,whiletheonlyinjuriesweremorepres- by the inhibitory action of beta-estradiol on the fungus,which inhib- ent in the oral mucosa, tongue and alveolar ridge.As in the present its the formation ofyeast cells of inhaled conidia and also modulates work,Brazão-Silvaetal.6 and Verli et al.10evaluatedonlyorallesions cellularimmuneresponses,besidesitslowinvolvementinagricultural and found multiple manifestation in most cases, the most frequent activities. It is interesting to remember that the primary infection oc- locations—gingiva and alveolar ridge, followed by the hard and soft cursinthelungs,whichmayconfoundthediagnosiswithtuberculosis. palate,buccalmucosaandtongue. However,patientscomplainmorecommonlyofdrycough,incontrast totuberculosiswhichisaccompaniedbyexudateandhaemoptysis. In conclusion, this study revealed that the epidemiology of paracoccidioidomycosis,includingthedemographicprofileofpatients Ingeneral,PCMhasbeenreportedinpatients,aged2-102years, andtheirclinicalpresentationsweresimilartoseveralotherseriesof buttheprevalenceisgreatestbetween30and60yearsoldandless cases,especiallyinBrazil.Thisisthemostimportantfungalinfection frequentduringthefirstdecadeoflifeandafterage70.3Theageof inLatinAmericaandtherecognitionoforallesionsisextremelyim- patientswithoralmanifestationsranged06-81yearsandtheaverage portant, as is often the first and in many cases the only manifesta- agewas49.66years.Somesimilarstudieshavefoundsimilarresults tionofthedisease.Moreover,increasinglyobservedcasesdiagnosed withaverageagethatalsofallintothefourthdecadeoflife,1,4,6,10,18 outside of rural areas due to increased urbanisation and away from whichcanbeexplainedbygreaterexposuretothefungusbyadultsin endemicareasrelatedtoglobalisationandtraveltoSouthandCentral theirworkactivities.Furthermore,itisbelievedthatthegreatmajority America. of the cases belongs to study chronic form of the disease which is seen in 90% of patients, it affects adults and often show secondary mucosallesions.3,6 ACKNOWLE DG M ENTS Withregardtopatientsskincolour,22(40.0%)wereAfrocaucasian, The authors thank the staff of Maxillofacial Pathology Laboratory 15(27.27%)whiteand12black(21.82%).Largecaseseriesshowedno oftheSchoolofDentistry,FederalUniversityofMinasGerais,Belo racial predisposition to the development of paracoccidioidomycosis. Horizonte,Brazilfortheirsupportinthisstudy. However,inaretrospectivestudywith1219patientsinBrazil,itwas observedthatblackandmulattoestendtohaveanincreasedprevalenceofacute/subacuteandwhitepatientsshowedapredominance 17 ofchronicdisease. TheassociationbetweenPCMwithhousinginruralareasandag- CO NFLICT O F INTE RE ST Therearenoconflictsofinterest. riculturalbusinessactivitiesisalsodescribedintheliterature.Paniago et al.4reportedthat45.5%of422patientswereruralworkers,Bicalho 1 et al. found this association in 53% of patients and Souza etal. 20 found that 65.2% lived in rural areas or working with agriculture. Although the medical records were incomplete in the profession of infectedpatients,sincesomeofthemdidnotinformtheprofession, itcanbeobservedthatthemajorityofthepatientswerefarmers(11 cases)andconstructors(6cases).Theseprofessionsarerelatedtothe exploitationofthesoil.SoilisthemainhabitatofP. brasiliensisandits filamentousformofinfectionisusuallyfoundinthesoilorleavesof plantsfacilitatingtheirinhalationbytheseprofessionals. Therearesomelaboratorydiagnosticmethodsofthedisease,including scaling analysis of the lesions, sputum or by biopsy. Paniago et al.4 emphasises that the diagnosis of ringworm when there are accessible lesion (skin, mucosa or superficial lymph node), the direct microscopicexaminationofmaterialobtainedfromlesionsshouldbe preferredforitssimplicityandaccuracy.Allthecasesinquestionwere diagnosedbyhistopathologicalexaminationofbiopsiedspecimensof REFERENCES 1. Bicalho RN, Espírito Santo MF, Ferreira de Aguiar MC, Santos VR. 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SouzaSP,JorgeVM,XavierMO.Paracoccidioidomycosisinsouthern RioGrandedoSul:aretrospectivestudyofhistopathologicallydiagnosedcases.Braz J Microbiol.2014;45:243-244. How to cite this article:TrindadeAH,MeiraHC,PereiraIF, deLacerdaJCT,deMesquitaRA,SantosVR.Oral paracoccidioidomycosis:Retrospectiveanalysisof55Brazilian patients.Mycoses. 2017;00:1–5.https://doi.org/10.1111/ myc.12622