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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
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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)
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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.
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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
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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