Clinicopathological characteristics of tumours of the intraoral minor salivary glands in 170 Brazilian patients

BritishJournalofOralandMaxillofacialSurgery54(2016)30–34

Clinicopathological characteristics of tumours of the intraoral minor salivary glands in 170 Brazilian patients

Aline Corrêa Abrahão

, Juliana de Noronha Santos Netto

, Fábio Ramôa Pires

, Teresa Cristina Ribeiro Bartholomeu dos Santos

, Márcia Grillo Cabral

aOralPathology,DepartmentofOralDiagnosisandPathology,FederalUniversityofRiodeJaneiroSchoolofDentistry,RiodeJaneiro,Brazil

bOralPathology,DepartmentofDiagnosisandSurgery,StateUniversityofRiodeJaneiroSchoolofDentistry,RiodeJaneiro,Brazil Accepted29October2015

Availableonline28November2015

Abstract

Tumoursoftheminorsalivaryglandsarerelativelyuncommon,andpublicationsfromaroundtheworldnormallyincludetumoursofboththe minorandmajorsalivaryglands,makingitdifficulttoassesstheirprevalenceanddistribution.Ouraimwastoevaluateretrospectivelythe clinicopathologicalfeaturesofaseriesoftumoursoftheintraoralminorsalivaryglandsfromtwouniversitiesinRiodeJaneiro,Brazil,and tocomparethedatawiththosefromotherepidemiologicalstudies.Atotalof170suchtumourswerediagnosedfrom1942to2012,andwere selectedfromtwouniversitydepartmentsoforalpathology.Eighty-nineofthetumourswerebenign(52%).Pleomorphicadenoma(n=75) andmucoepidermoidcarcinoma(n=23)werethemostcommonbenign(44%)andmalignanttumours(14%),respectively.Therewere104 femalepatients(61%)andbothbenignandmalignanttumoursaffectedmorewomenthanmen.Significantlymoretumourswereinthepalate (n=95,56%;p=0.001).WeconcludethatthesetumourshadfeaturessimilartothosefromotherstudiesfromNorthandLatinAmerica,but differfromtheresultspresentedfromAsia.Furtherstudiesshouldbedesignedtohighlightpossiblegeographicalandpopulation-specific characteristicsofthesetumours.

©2015TheBritishAssociationofOralandMaxillofacialSurgeons.PublishedbyElsevierLtd.Allrightsreserved.

Keywords:Minorsalivarygland;Tumours;Neoplasms;Pleomorphicadenoma;Mucoepidermoidcarcinoma.

∗Correspondingauthorat:FederalUniversityofRiodeJaneiroSchool ofDentistry,DepartmentofOralDiagnosisandPathology,AvenidaPro- fessorRodolphoPauloRocco,325–1^◦andar,CidadeUniversitária–Rio deJaneiro,RiodeJaneiro-Brazil,ZipCode:21941-913.Tel./fax:+5521 3938-2071.

E-mail addresses: alineabrahao@odonto.ufrj.br (A.C. Abrahão), julianansn@yahoo.com.br(J.d.N.S.Netto),ramoafop@yahoo.com (F.R.Pires),tcnath@terra.com.br(T.C.R.B.d.Santos),

marciagrillo@odonto.ufrj.br(M.G.Cabral).

1 AvenidaProfessorRodolphoPauloRocco,325–1^◦ andar.Cidade Universitária–RiodeJaneiro,RiodeJaneiro–Brazil.ZipCode:21941-913.

Tel.:+55213938-2071.

2 Boulevard28deSetembro,157sala503.VilaIsabel–RiodeJaneiro, RiodeJaneiro,Brazil.ZipCode:20551-030.Tel.:+55212868-8284.

Introduction

Tumoursoftheminorsalivaryglandsarerelativelyuncom- monneoplasmsoftheheadandneck.^1,2Specificdataabout their incidence and clinicopathologicalfeatures are some- times difficulttoretrieve,asmanystudiesincludetumours of bothmajorandminorsalivaryglandsormalignantneo- plasms alone.^3,4 During the last15 years therehave been severalpublishedstudiesoftumoursthataffectonlytheminor salivaryglands,butfewhaveincludedBrazilianpatients,^5,6 thoughpreviousepidemiologicaldatahaveshownthatclin- icopathologicalcharacteristicsofthesetumoursvaryamong populations.^7,8Thesedatareinforcetheimportanceofmore specific studies designed to understand their profile. It is accepted that pleomorphic adenoma and mucoepidermoid

http://dx.doi.org/10.1016/j.bjoms.2015.10.035

0266-4356/©2015TheBritishAssociationofOralandMaxillofacialSurgeons.PublishedbyElsevierLtd.Allrightsreserved.

Table1

Distributionandratios(:)ofbenign:malignantintraoraltumoursoftheminor salivaryglandsbydecades.Dataarenumberornumber(%).

Decade Benign Malignant Benign:malignant Total

1950 4 0 1:0 4(2)

1960 1 2 1:2 3(2)

1970 8 4 1:0.5 12(7)

1980 5 3 1:0.6 8(5)

1990 7 5 1:0.7 12(7)

2000 51(55) 41(45) 1:0.8 92(54)

2010 13(33) 26(67) 1:2 39(23)

Total 89(52) 81(48) 1:0.9 170

carcinoma are the most common intraoral tumours of the minor salivary glands, but it is still difficult to calculate theincidenceofotherbenignandmalignantsalivarygland tumoursbecausetheyaresorare.⁷

The purpose of the present study was to evaluate ret- rospectively the clinicopathologicalfeatures of aseries of thetumoursfromtwopublicuniversitiesinRiodeJaneiro, Brazil,andcomparethesedatawiththosefromstudiesfrom othercountries.

Patientsandmethods

The files of two public oral pathology services in Riode Janeiro,Brazil(School of Dentistry, FederalUniversity of RiodeJaneiroandSchoolofDentistry,StateUniversityof Riode Janeiro)were reviewed andall casesdiagnosedas intraoraltumoursoftheminorsalivaryglandswereretrieved.

Histological slides containing 5␮m-sections stained with haematoxylinandeosinfromeachcasewerereviewedunder lightmicroscopy,andallinwhichthefinaldiagnoseswere confirmedwereselected.Clinicopathologicaldataincluding

age,sex,anatomicalsiteofthetumour,andhistologicaltype wererecordedfrompaperrecordsthatwereretrievedfrom thelaboratories.Allhistologicalslideswereanalysedbythree oftheauthorstoconfirmthediagnosisaccordingtocriteria laiddowninreferencetexts.^1,2Whenneeded,specialstains (mucicarmineandperiodicacid-Schiff)wereusedtoaidin thefinaldiagnosis.Casesforwhichwehadnorepresentative sectionsoftissueorthathadbeendiagnosedexclusivelyby fine-needleaspirationbiopsywereexcluded,asweretumours in whichthe finaldiagnosis could not be characterisedin moredetailthan“adenoma”or“adenocarcinoma”,orwhen clinicopathologicalinformationwasnotavailable.Thosethat hadmorethanonebiopsy(incisionalandexcisionalbiopsy specimens)wererecordedonlyonce.

StatisticalanalysesweremadewiththeaidofIBMSPSS software(version20,IBMCorp,Armonk,NY),andthechi squaretestandStudent´sttestwereused toassessthesig- nificanceofdifferences,asappropriate.Probabilitiesofless than0.05wereacceptedassignificant.

Results

Atotalof174tumourswereselected,andfourwithincon- clusivefinaldiagnoseswereexcluded,leaving170casesof which108werediagnosedintheOralPathologyLaboratory, FederalUniversity of RiodeJaneiro (0.8%of allbiopsies recordedinthelaboratory)and62intheOralPathologyLabo- ratory,StateUniversityofRiodeJaneiro(1.3%ofallbiopsies recordedinthelaboratory).Onhistologicalclassification89 tumourswerebenign(52%)and81weremalignant(48%).

Theratioofbenign:malignanttumourswashigherthrough- out most of the decades, withthe exception of the 1960s andthe2010s(Table1).Table2 showstheincidence,and

Table2

Comparativeincidence,sex,andmean(SD)agedistributionaccordingtohistologicalsubtypesof170intraoralminorsalivaryglandtumours.

Histologicalsubtype No %ofGroup %ofTotal Sex(%) Mean(SD)age(years)

Male Female

Benignintraoralminorsalivaryglandtumours:

Pleomorphicadenoma 75 84 44 41 59 45(20)

Cystadenoma 9 10 4 33 67 61(19)

Canalicularadenoma 3 4 2 33 67 54(9)

Basalcelladenoma 1 1 1 0 100 60

Myoepithelioma 1 1 1 100 0 NS^*

Total 89 100 52 40 60 47(20)

Malignantintraoralminorsalivaryglandtumours:

Mucoepidermoidcarcinoma 23 28 14 35 65 52(19)

Polymorphouslow-gradeadenocarcinoma 21 26 12 29 71 60(12)

Adenoidcysticcarcinoma 19 24 11 47 53 56(19)

Adenocarcinoma,nototherwisespecified 6 7 4 33 67 58(16)

Basalcelladenocarcinoma 4 5 2 25 75 49(8)

Carcinomaex-pleomorphicadenoma 4 5 2 50 50 45(22)

Aciniccelladenocarcinoma 3 4 2 33 67 57(20)

Mucinousadenocarcinoma 1 1 1 100 0 74

Total 81 100 48 37 63 55(17)

Total(benignandmalignant) 170 100 100 39 61 51(19)

∗NS=notstated.

Table3

Distributionaccordingtohistologicalsubtypeandanatomicalsiteof170tumoursoftheintraoralminorsalivaryglands.Dataarenumberornumber(%).

Histologicalsubtype Siteoftumour

Palate Buccalmucosa Upperlip Floorofmouth Alveolarridge Others Total Benigntumours:

Pleomorphicadenoma 48(64) 11(15) 10(13) 1(1) 2(3) 3(4) 75

Cystadenoma 0 4 3 1 0 1 9

Canalicularadenoma 0 1 2 0 0 0 3

Basalcelladenoma 0 0 1 0 0 0 1

Myoepithelioma 0 0 0 0 0 1 1

Total(benign) 48(54) 16(18) 16(18) 2(2) 2(2) 5(6) 89

Malignanttumours:

Mucoepidermoidcarcinoma 13 4 2 1 2 1 23

Polymorphouslow-gradeadenocarcinoma 16 2 1 0 1 1 21

Adenoidcysticcarcinoma 8 3 1 5 2 0 19

Adenocarcinoma,nototherwisespecified 3 0 0 1 2 0 6

Basalcelladenocarcinoma 2 1 1 0 0 0 4

Carcinomaex-pleomorphicadenoma 4 0 0 0 0 0 4

Aciniccelladenocarcinoma 0 1 1 0 1 0 3

Mucinousadenocarcinoma 1 0 0 0 0 0 1

Total(malignant) 47(58) 11(14) 6(7) 7(9) 8(10) 2(2) 81

Total 95(56) 27(16) 22(13) 9(5) 10(6) 7(4) 170

sexandagedistributionaccordingtohistologicalsubtypes.

Mucoepidermoidcarcinomaswereadditionallysubclassified intolow-grade(30%),intermediategrade(48%),andhigh- gradetumours(22%),accordingtoEllisandAuclair.²

Table3 shows the distributionof tumoursaccording to histological subtype and site. There was a significant dif- ferenceintheanatomicaldistributionofthetumourswhen thewholesamplewascompared(p=0.001),buttherewere nosignificant differencesinthe distributionofthe typeof tumours(benignandmalignant), histologicalsubtype, and anatomicalsitesbetweenthesexes(Table4).

Discussion

Intraoral tumours of the minor salivary glands account for 12%-30%of allneoplasmsof the salivaryglands^1,8–11

Table4

Sexdistributionaccordingtothetumourgroup,mostcommonhistological subtypesandanatomicallocationofthetumours.Dataarenumber(%).

Variable Sex pvalue

Male Female

Typeoftumour: 0.648

Benign 36(40) 53(60)

Malignant 30(37) 51(63)

Histologicaltype: 0.891

Pleomorphicadenoma 31(41) 44(59) Mucoepidermoidcarcinoma 8(35) 15(65) Polymorphouslow-grade

adenocarcinoma

6(29) 15(71) Adenoidcysticcarcinoma 9(47) 10(53)

Siteoftumour 0.837

Palate 37(39) 58(61)

Buccalmucosa 10(37) 17(63)

Upperlip 8(36) 14(64)

Floorofthemouth 5(56) 4(44)

Alveolarridge 3(30) 7(70)

and 0.4%-1.9% of all biopsies in oral pathology laboratories.3,7,8,12–15Somehistologicaltypesarerare,and specificsubtypesshowapredilectionforinvolvementwith the minorsalivaryglands.Recent publicationshaveshown thatmalignanttumoursaremorelikelytodevelopinminor ratherthanmajorsalivaryglands.^4,9,10

Thetrueincidenceandtheclinicopathologicalcharacter- istics of tumoursof the minorsalivaryglandsare difficult toascertain,because moststudiesinclude tumoursinboth major and minor salivary glands. The source of the sam- pleisabiasthatmayinfluencethereportedprevalencefor site. Whilegeneralhospitals commonlyreceivespecimens ofmajorsalivaryglandtumours,oralpathologylaboratories anddentalschoolstendtodealwithbiopsyspecimensfrom intraoralsalivaryglands(Table5).^3,11,16,17

Ourresultsshownanalmostequivalentnumberofbenign (n=89)andmalignant(n=81)tumours,whereasmoststud- iesfromNorthandLatinAmericancountrieshavereported a predominance of benign tumours.3,5,7,12,19 In contrast, seriesreportedfromAfrican,European,andAsiancountries predominantly describemalignant tumours.8,14–17,21–25 An exceptiontothisisJapan,wherebenigntumoursaremore prevalent (Table 5).^13,18 Geographical variations seem to exist, but the ratio of benign:malignant tumours is also dependent onthesourceofthestudy.Asexpected,studies from departments of oncologyandhead andneck surgery reportmoremalignanttumours.^6,16,17

Pleomorphic adenoma is the most common reported such tumour, making up 16%-66% of all neoplasms.3,5,7,8,11–14,18,19 In general, studies that report large series of malignant tumours agree that mucoepi- dermoid carcinomas (25%-41%)^6,15,20,21 and adenoid cystic carcinomas (15%-45%)^8,15–17,22 are the two most common malignant subtypes. Curiously, polymorphous low-grade adenocarcinomahas beenreportedless oftenin

Table5

ClinicopathologicalcharacteristicsofintraoralminorsalivaryglandtumoursincludedinepidemiologicalstudiespublishedinEnglishsince1995.

Firstauthorand reference

Year Country Source* N** Tumours(%) Meanage

(years)

M:F***

ratio

Histologicalsubtype (%)****

Benign Malignant PA MEC ACC

Loyola⁵ 1995 Brazil Oral 164 62 38 41.5 1:1.3 53 17 13

Rivera-Bastidas¹² 1996 Venezuela Oral 62 55 28 NS***** 1:1.8 39 29 10

Kusama¹³ 1997 Japan Oral 129 62 38 47.1 1:1.4 57 19 13

Lopes⁶ 1999 Brazil Other 196 35 65 NS 1:1 33 39 17

Jansisyanont²⁰ 2002 UnitedStates Oral 80 24 76 NS 1:1.6 21 41 9

Toida¹⁸ 2005 Japan Other 82 67 33 51.4 1:1.9 66 10 12

Yih¹⁹ 2005 UnitedStates Oral 213 56 44 NS 1:1.9 44 21 10

Jaber²¹ 2006 Libya Oral 75 39 61 44.1 1:1.4 31 25 17

Buchner³ 2007 UnitedStates Oral 380 59 41 NS 1:1.7 39 22 6

Pires⁷ 2007 UnitedStates Oral 546 56 44 60.2 1:1.6 33 23 6

Wang⁸ 2007 China Oral 737 46 54 NS 1.1:1 38 12 19

Copelli²³ 2008 Italy Oral 43 — 43 53.9 1:1 — 27.9 60.6

Dhanuthai¹⁴ 2009 Thailand Oral 311 47 53 41.6 1:1.4 43 23 18

Adeyemi²² 2010 Nigeria Other 92 38 62 44.7 1:1 33 12 38

Jaafari-Ashkavandi¹¹ 2011 Iran Other 82 54 46 41.4 1:1.3 44 12 28

Venkata¹⁵ 2011 India Oral 185 25 75 46.1 1.1:1 22 34 15

Vaidya¹⁶ 2012 India Other 104 16 84 45 1:1 16 18 45

Wyszynska-Pawelec¹⁷ 2012 Poland Other 57 37 63 NS 1:1.8 30 14 32

Dalgic²⁵ 2014 Turkey Oral 23 48 52 31.3 2.3:1 30 50 50

Ramesh²⁴ 2014 India Oral 30 8 22 44.2 1:2 87.5 68.2 27.3

Presentstudy 2014 Brazil Oral 170 52 48 51 1:1.6 44 14 11

* Oral=oral pathology services; Other=other sources; ** Total number of patients; *** M=male; F=female; **** PA=pleomorphic adenoma;

MEC=mucoepidermoidcarcinoma;ACC=adenoidcysticcarcinoma;and*****NS-notstated.

studies from Asia and Europe8,11,14,16–18 than in studies from America, ^3,7,20 possibly because of geographical differences in specific subtypes of tumour, although the numberofbiopsyspecimensanddifficultiesinclassification must also be considered. The present results indicate that pleomorphicadenomas make up 44% of the tumours that wefound,followedbymucoepidermoidcarcinomas(14%), polymorphous low-grade adenocarcinoma (12%), and adenoidcysticcarcinomas(11%)(Table2).Othermalignant variantsthat occurred lessoftenwere adenocarcinomanot otherwiseclassified,basalcelladenocarcinoma,carcinoma ex-pleomorphicadenoma,aciniccelladenocarcinoma,and mucinousadenocarcinoma,whichissimilartootherstudies from North and Latin America (Table 5). No carcinomas ofthesalivaryductwerefound.However,thesehavebeen reportedtobemorecommoninthemajorsalivaryglands.² Intheminorsalivaryglandstheyaccountsforlessthan2%

of the malignant subtypes.^6,15 In general, throughout the decades,benigntumoursweremoreprevalent.However,dif- ferencesinthebenign:malignantratiowerenotremarkable (Table1).

Thirteenof20previousstudiesthatconcentratedonthese tumoursreportedsince1995haveshowedfemalepredom- inance(Table 5), as didwe. Women outnumberedmen in themainhistologicalsubtypesexceptadenoidcysticcarci- noma.Thispredilectionisusuallyseeninbothbenignand malignanttumoursoftheminorsalivaryglands,thoughsome studieshaveshownthatmalignanttumoursaremorecommon inmen.6,8,15,18,22Inpreviousreportsthemeanageofpatients affectedbythesetumourswasinthefifthtosixthdecadesof

life(Table5),whileinBrazilianseries,theyweremorecom- moninadultsintheir forties.^4,5,9In general,patients who developbenigntumoursareusuallyyoungerthanthosewho developmalignantones,aswefound.5–8,11–15,18,22Whenthe mostcommonhistologicalsubtypesareanalysedspecifically, itisalsopossibletoobservethatthemeanageofthepatients with pleomorphic adenomas is usually lower than that of patientswithmucoepidermoidcarcinomasandadenoidcystic carcinomas,aswefound.3,5,7,13,15,18,19,22

Itisacceptedthatthesetumoursaremostlikelytodevelop inthepalate,followedbythebuccalmucosaandtheupper lip.3,5,7,8,12,18–21 Our results confirm these data and rein- forcethefactthattherearesomestrikingdifferencesintheir anatomicaldistribution.Otherseriesthatincludedpredomi- nantlymalignanttumourshaveshownthatsitessuchasthe alveolarmucosa(includingtheretromolararea)andthefloor ofthemouthcanfollowthepalateasthesitesmostlikelyto beaffected.^6,13–16,24

The clinicopathological features of the present series are similarto those reportedby other studies from North and Latin America, and differ from most reports from Asia, Africa, and Europe. Further studies from different places are encouraged to highlight the possible geo- graphical and population-specific characteristics of these tumours.

ConflictofInterest

Wehavenoconflictsofinterest.

Ethicsstatement/confirmationofpatients’permission

TheprotocolofthestudycompliedwiththeDeclarationof Helsinki.Patients’permissionwasnotrequiredasweused onlylaboratoryslidesandanonymisedrecords.

Financialsupport

This work was supported by FAPERJ (Grant E26/

111.643/2010)andCNPq.

Acknowledgements

The authors would like to thank FAPERJ (Grant E26/

111.643/2010)and CNPqfor the financial supportto this study.

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