Streptococcus bovis endocarditis: analysis of cases between 2005 and 2014

braz j infect dis.2015;19(2):209–212

ww w . e l s e v i e r . c o m / l o c a t e / b j i d

The

Brazilian

Journal

of

INFECTIOUS

DISEASES

Brief

communication

Streptococcus

bovis

endocarditis:

analysis

of

cases

between

2005

and

2014

Renato

Mello

_,

_Marisa

_da

_Silva

_Santos

_,

_Wilma

_Golebiosvki

_,

Clara

Weksler

_,

_Cristiane

_Lamas

a_{Unigranrio,RiodeJaneiro,RJ,Brazil}

b_{InstitutoNacionaldeCardiologia,RiodeJaneiro,RJ,Brazil}

c_{InstitutoNacionaldeInfectologiaEvandroChagas,Fiocruz,RiodeJaneiro,RJ,Brazil}

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received10October2014 Accepted16December2014 Availableonline27January2015

Keywords:

Infectiveendocarditis

Streptococcusbovisgroup

Cardiacsurgery Coloniclesions

a

b

s

t

r

a

c

t

Background:Streptococcusbovisisaclassicaletiologyofendocarditisandisassociatedwith

coloniclesions.NoseriesofcasesfromBrazilhasbeendescribed.

Objectives: TodescribeaspectsofS.bovisendocarditis.

Methods:Thisisacaseseriesofpatientsadmittedtoacardiacsurgeryreferralcenter,

dur-ingtheyears2005–2014.Clinical,laboratory,echochardiographic,colonoscopic,treatment, surgicalandoutcomevariableswerestudied.

Results:NinepatientswithS.bovisendocarditiswereincluded;allcasesfulfilledthemodified

Dukecriteria.Incidencewas8/220(4%)inyears2006–2014.Thereweresevenmaleand twofemalepatients;meanagewas56.7years,standarddeviation13.4.Allpatientshad nativeaorticvalveinvolvement.Presentationwassubacutein7/9(71%).Feverwaspresent in7/9(77.7%),emboliclesionstosolidorgansoccurredinthree,andperivalvularabscess intwopatients.Allechocardiogramsshowedmoderatetoseverevalvularregurgitationand vegetations.Microcyticanemiawasseenin7/7patients.Colonoscopyshowedabnormal findingsin7/9(77.7%).Surgerywasindicatedfor6/9patientsduetoacuteaorticregurgitation andleftventricularfailure.Allpatientsweredischargedhome.

Conclusions: S.bovismostfrequentlyaffectedtheaorticvalveofmalepatients.Colondisease

wasfrequent.Surgerywasindicatedfrequentlyduetohemodynamiccompromise. ©2015ElsevierEditoraLtda.Allrightsreserved.

S.bovisendocarditisisaclassical,but uncommoncause of

infectiveendocarditis(IE).TheassociationofS.bovisIEand colon carcinoma has long been established. Several other colonic,non-neoplasticconditionshavebeenattributedtoS.

∗ _{Correspondingauthorat:InstitutoNacionaldeCardiologia,8}◦_{andar,enfermariaOrovalvar,RuadasLaranjeiras374,Laranjeiras,Riode}

Janeiro,CEP22240-006,Brazil.

E-mailaddress:[email protected](C.Lamas).

bovissuchasadenomatouspolyps,hyperplasticpolypsand

diverticulardisease,adenomatouspolypspredominating, cor-respondingto53%ofcases.1_{Theseevidenceshaveestablished} theneedtoinvestigatecolonorliverdiseaseinallpatients

http://dx.doi.org/10.1016/j.bjid.2014.12.007

210

presentingwith S. bovis bacteremiaand/or endocarditis. S.

bovisbacteremiaisamajorcriterionforinfectiveendocarditis2

andechocardiogramsaremandatoryinthisclinicalscenario. RecentstudieshavesuggestedanewnomenclatureforS.

bovis,sothatS.bovisbiotypeIisnownamedStreptococcus

gal-lolyticus,biotypeII.1correspondstoStreptococcusinfantarius,

andbiotypeII.2toStreptococcuspasteurianus.Inthis respect,

the“S.bovis”mostcommonlyassociatedwithcoloniccanceris

currentlyidentifiedasS.gallolyticusbiotypeI;thisisthespecies usuallyisolatedfrombloodculturesinthissituation.3 How-ever,theroutineclinicalmicrobiologylaboratorystillreports

“S.bovis”only.

A large case series evaluating 2781 cases of definite IE inadults,fromvarioussites,intheInternational Collabora-tionStudyonInfectiveEndocarditis-prospectivecohortstudy, intheyears 2000–2005,hasshowngeographicaldifferences betweentheincidenceofS.bovisIE.4_{Itcorrespondedto9/597} (2%)ofcasesinNorthAmerica,17/254(7%)inSouthAmerica, 116/1213(10%)ofcasesinEurope,and23/717(3%)ofcasesin othersites(Africa,MiddleEast,Asia).Despitethereference to13casesofS.bovisIEin300(4.3%)Brazilianpatientswith IEinaseriespublishedin1990,noanalysisofthisgroupof patientswasprovided.5_{TworecentBrazilianseriesofIEwith} 62and64cases,respectively,didnotfeatureS.bovisasan eti-ologicagent.6,7_{Thegoalofthepresentstudywastodescribe} thefeaturesofaseriesofcasesofIEinaBrazilianscenario, establishingacomparisontowhatisknownfromthe litera-ture.

Thisisaprospectivecaseseriesstudyofpatients admit-tedtoInstitutoNacionaldeCardiologia(INC),RiodeJaneiro, Brazil,betweenthe years of2005 and 2014.Adultpatients withdefiniteIE,accordingtothemodifiedDukecriteria8_were included.INCisacardiacsurgeryreferralhospital,receiving alargenumberofcaseswithIEwho haveanindicationfor surgery.EthicalapprovalwasobtainedfromtheEthics Com-mitteeofINCunderthenumber080/2005.Informedconsent wasobtainedforall patients.Thestudy protocol conforms to the ethical guidelines of the 1975 Helsinki Declaration asreflectedinapriori approvalbytheinstitution’s human researchcommittee.

IncidenceofS.bovisIEwasdetermined,aswellas demo-graphic data, clinical presentation, affected valves, routine laboratoryandechocardiographicdata,complications, pres-ence of comorbidities, associated liver or colonic disease, surgeryandmortality.IdentificationofS.boviswasdoneby automatedmethods(VITEKIIsystem)andnobiotypingwas available.Descriptivestatistics,usingfrequenciesas percent-agesandmeanandstandarddeviation(SD)wascomputedon Excel®_charts.

Ninecases ofS. bovis IE were seen inthe study period (2005–2014). All cases were referred from other hospitals. Thereweresevenmaleandtwofemalepatients;agerange was26–70years,mean±SDwas56.7±13.4years.Allpatients presentedaorticvalveinvolvement,although twoalsohad themitralvalveaffectedandonethetricuspidvalve.Clinical presentationwassubacutein7/9patientsandacutein2/9.

Inthe pastmedicalhistory, threepatients hadprevious abdominalsurgery,twohadchronicliverdisease,threehad previousIE,twohadcongestiveheartfailure,andtwohada historyofrheumaticfever.Oneoutofsixwasaheavydrinker,

threedrank“socially”;onewasasmoker.Threeofthenine patientsalreadyhadapreviousdiagnosisofcoloncarcinoma (four,fiveandsixyearspriortothepresentepisodeofIE).

Fever was seen in 7/9 (77.7%), newly diagnosed splenomegaly in two out of six patients (33.3%). Embolic phenomenawereseenin3/9patients(splenicinfarctinone, splenic abscessintwo).Two ofnine patients had intracar-diac abscesses.No patientshad persistently positive blood cultures,persistentsepsis,orosteoarticularcomplications.

C-reactiveproteinlevelswereelevatedin3/7cases(42.8%) anderythrocytesedimentationrateinfour(57%,4/7).Ferritin levelswerewithinnormalrangeintheeightcasesinwhomit wasmeasured,althoughhemoglobinlevelwaslowinall7/7 patientswhoitdetermined.Meanhemoglobinwas10.22and meancorpuscularvolumewas77.6fl.

Transthoracic echocardiograms (TTE) were done in two patients and transesophageal scans in seven; moderate to severe valvular regurgitation and vegetationswere seen in allscans.Majorechocardiographiccriteriawerepresentinall patients,twobyTTEandsevenbyTEE.

Allpatientsweresubmittedtocolonoscopy,and7/9(78%) had abnormalfindings:threecoloncarcinomas, four diver-ticulardiseaseofthecolon(polypswerepresentinthreeof these).

Antibiotictreatmentwasgivenforfourtosixweeks,and consistedofpenicillinin5/9cases,andampicillinin4/9; gen-tamicinwasgivenincombinationinsixcases.

Surgery was indicated in6/9 casesdue tosevere aortic regurgitationand/orheartfailure.

Allpatientsweredischargedalivefromtheindex hospital-ization.

Table1summarizesthemainclinicalandlaboratory char-acteristicsofthecases,andcomparesthemtootherpublished series. Papersselectedforcomparisonwerethosereporting seriesofpatientswithS.bovisIEafterthe1980s.

S.bovisgroupcolonizesthehumangastrointestinaltract.

Itispresentin2.5–15%ofhealthyindividualsandin29–55% of patients with inflammatory bowel disease and colon carcinoma.Itreachesthebloodstreambypenetratingthe gas-trointestinalmucosa, whichisfacilitatedbybreachesasin inflammationorneoplasia.S.bovisgroupaccountsfor approx-imately 7%ofnative valveIEinnon-drug users and5%in patientswithprostheticvalveIEinthelargestpublishedseries so far.4 _{However, theincidence ofS.bovis IEvaries greatly} bygeographicalarea,inthissamereport.Allmajorseriesof IEreportedsofararefromEurope,whereincidenceisabove 10%.9–17_{AlthoughS.bovisfeaturesinsomeseriesofIEfrom} Brazil,ithasnotbeenstudiedasasingleentity,soastoverify differencesorsimilaritiestotheliterature.

IE in Brazil, a developing country, affects both young patients, with rheumatic heart valve disease, and older patients,whomayhaveunderlyingcolonicpathology.Inour institution, incidenceofS.bovisIE was4%inrecentyears, which issimilar toarecentlypublishedseries ofIE.18 _This may reflectthelowpositivityratesofbloodcultures, espe-cially becauseofpriorantibioticuse. InBrazil,purchaseof antibioticswasrestrictedtomedicalprescriptiononlyafter 2011, and over-the-counter sale ofantibioticswas the rule untilthen.AntibioticusewouldrapidlyclearS.bovisfromthe bloodstream,asitisverysensitivetopenicillin.6,7,19

b r a z j i n f e c t d i s . 2 0 1 5; 1 9(2) :209–212

211

Table1–ComparisonofvariablesfromrecentcaseseriesofS.bovisinfectiveendocarditis.

A B C D E F G H I J

Brazil France France France Germany Italy Italy Spain Spain Ireland

Studyperiod 2005–2014 1980–1991 1987–1992 1993–2001 1983–1996 1990–2003 1990–2003 1988–2005 1997–2008 2000–2009

NumberofS.bovisIE 9 53 32 40 22 22 30 55 16 7

%numberS.bovis/totalIE 9/201(4%) 53/482(11%) N/D 40/206(19%) 22/265(8%) N/D 30/199(15%) 55/228(24%) N/D N/D

Ageaverage(standarddeviation) 56.7(13.4) 60.6(12.2) 61.3(5) 64(12) 67(range

49–76)

59.5 58.6(12.4) 66 69.5(11.8) 70.9(8.6)

Male,n(%) 7(77.7%) 42(79.2%) 27(84%) 34(85%) 12(54%) 17(77.6%) 17(77.2%) 51(93%) 9(56.3%) 5(71.4%)

Female,n(%) 2(22.3) 11(20.8%) 5(15%) 6(15%) 10(46%) 5(22.4%) 5(22.8%) 4(7%) 7(43.6%) 2(28.6%)

Siteofinfection

Nativemitralvalve 0(0%) 6(11%) N/D 7(17%) N/D 3(13%) 4(13%) 10(18%) N/D 1/7(14%)

Nativeaorticvalve 6(66.6%) 26(49%) N/D 15(37%) N/D 9(26%) 8(27%) 22(40%) N/D 0(0%)

Nativemitro-aorticvalves 2(22.2%) 18(33%) N/D N/D N/D 7(40%) 12(40%) 23(42%) N/D 1/7(14%)

Prostheticvalve 0(0%) 0(0%) N/D 5(12%) N/D 2(10.0%) 3(10%) 0(0%) 10/16(62.5%) 3/7(43%) Tricuspidvalve 0(0%) 1(1.8%) N/D 2(5%) N/D 1(6.7%) 2(7%) 0(0%) N/D 0(0%) Clinicalaspects Heartfailure 1(11.1%) 35/53(66%) ND 8/40(20%) 7/22(32%) ND 12(40%) 15(27%) ND 2(28.6%) Embolism 2/6(33.3%) 22/53(42%) ND 22(55%) 2/22(9%) ND ND 21(38%) 2(13%) 0 Surgery 6(66.6%) 41/53(77%) ND 22(55%) 16/22(73%) ND 22(73%) 19(29%) 6(38%) 2(28.6%) Colonoscopy

Patientswithcolonoscopy 9(100%) 40/53(75%) 32/32 40/40 ND 18/22(82%) 27/30(90%) 46/55(84%) 15/16(94%) 7(100%)

Patientswithpositivecolonoscopy 7(77.7%) 27(67%) 18(56.2%) 22(56%) ND 8(%) 4(15%) 29(63%) 14(93.0%) 6(85.7%)

In-hospitalmortality 0(0%) 4(7.5%) N/D 1(2%) ND ND 5(16.7%) 12(22%) 2(12.5%) 0(0%)

A–presentstudy,adaptedfromreferences:B–Balletetal.(1995);C–BrunoHoenetal.(1994);D–Pergolaetal.(2001);E–Kupferwasseretal.(1998);F–Tripodietal.(2005);G–Tripodietal.(2004);H –Corredoiraetal.(2008);I–Fernández-Ruizetal.(2010);J–Fitzmauricetal.(2013).

212

S.bovisIEusuallyaffectspatientsolderthan60years;mean

ageinourstudywas56.7years.Itmoreoftenaffectsthe aor-ticvalve,andthiswasthecaseinallourpatients,although thereisareferralbias,sinceINCisasurgicalhospitaland hemodynamiccompromiseismoresevere whenthe aortic valveis affected.However, aorticvalve involvement,alone orcombinedwiththemitralvalve,withhighrates(55–77%) ofsurgeryindicationwasseeninlargerseriesfromFrance, ItalyandGermany.9–12_{Astrongassociationwithcolonic} can-cerhasbeenrecognizedforS.bovisbiotypeI,orS.gallolyticus.20 However,coloniclesionsfoundinassociationwithS.bovisIE maybeneoplasticornon-neoplastic.Itisbelievedthecolonic lesion facilitatescolonizationbyS. bovis, providesa physi-calbreachinthemucosa,and thereforemakesbacteremia more likely. On the other hand, S. bovis may have tumor promotingpropertiestocoloniclesions,viaproinflammatory (cyclo-oxygenase2)pathways.Incidenceofcoloncarcinoma

andIEbyS.bovishasbeenestimatedas18–62%,anditwas

presentinthreeoutofninepatientsinthisseries.Bacteremia orendocarditismayprecedeorfollowcoloncarcinoma.Three oftheninepatientsinourstudyalreadyhadaprevious diag-nosisofcoloniccancer.

Arecentmeta-analysiswasconductedtodeterminethe riskassociatedwithStreptococcusbovisinfectionandthe occur-renceofcolorectalneoplasia.21 Studiesincludedwerethose

onS.bovissepticemia,S.bovisendocarditisandS.bovisfecal

carriage.Overall,thepresenceofS.bovisinfectionwasfound tobesignificantlyassociatedwiththepresenceofcolorectal neoplasia.S.bovisendocarditisshowedthestrongest associ-ationinanalysesofcase-controlstudiesandcaseseries(OR 14.54,95%CI5.66–37.35).

Despitethesmallnumberofcasesinthisseries,itisthe firstseriesofS.bovisIEdescribingpatientsfromLatinAmerica. TheclinicalprofileofS.bovisIEandassociatedcolondisease wassimilartootherrecentlypublishedseriesfrom Europe. Similaritiesarethemeanageof60years,thepredominance ofaorticvalveinvolvement,highproportionofsurgery indi-cation,andthefindingofcolonicpathologyinmostpatients.

Conflicts

of

interest

Theauthorsdeclarenoconflictsofinterest.

Acknowledgements

Wethankallthemedicalandnon-medicalstaffwhohelped lookingafterthepatientspresentedinthisstudy.

Dr. Lamas thanks FUNADESP/Unigranrio for a personal grantthathelpedherinherendocarditisresearch.

r

e

f

e

r

e

n

c

e

s

1. GoldJS,BayarS,SalemRR.AssociationofStreptococcusbovis bacteremiawithcolonicneoplasiaandextracolonic malignancy.ArchSurg.2004;139:760–5.

2. DurackDT,LukesAS,BrightDK,DukeEndocarditisService. Newcriteriafordiagnosisofinfectiveendocarditis:utilization ofspecificechocardiographicfindings.AmJMed.

1994;96:200–9.

3.RichardF.WhathappenedtotheStreptococci:overviewof taxonomicandnomenclaturechanges.ClinMicrobiolRev. 2002;15:613–30.

4.MurdochDR,CoreyGR,HoenB,etal.Clinicalpresentation, etiology,andoutcomeofinfectiveendocarditisinthe21st century:theInternationalCollaborationon

Endocarditis-ProspectiveCohortStudy.ArchInternMed. 2009;169:463–73.

5.MansurAJ,GrinbergM,GallucciSD,BellottiG,JateneA, PileggiF.Endocarditeinfecciosa:análisede300episódios.Arq BrasCardiol.1990;54:13–21.

6.NunesMCP,GalapeCL,FerrariTCA.Profileofinfective endocarditisatatertiarycarecenterinBrazilduringa seven-yearperiod:prognosticfactorsandin-hospital outcome.IntJInfectDis.2010;14:e394–8.

7.RibeiroDGL,SilvaRP,RodriguesSobrinhoCRM,etal.Infective valveendocarditistreatedbysurgery:analysisof64cases. RevBrasCirCardiovasc.2005;20:75–80.

8.LiJS,SextonDJ,MickN,etal.Proposedmodificationstothe Dukecriteriaforthediagnosisofinfectiveendocarditis.Clin InfectDis.2000;30:633–8.

9.BalletM,GevigneyG,GareJP,DelahayeF,EtienneJ,Delahaye JP.InfectiveendocarditisduetoStreptococcusbovis–areportof 53cases;1995.

10.PergolaV,SalvoGD,HabibG,etal.Comparisonofclinicaland echocardiographiccharacteristicsofStreptococcusbovis endocarditiswiththatcausedbyotherpathogens.AmJ Cardiol.2001;88:871–5.

11.KupferwasserI,DariusH,MüllerAM,etal.Clinicaland morphologicalcharacteristicsinStreptococcusbovis endocarditis:acomparisonwithothercausative microorganismsin177cases.Heart.1998;80:276–80.

12.TripodiMF,AdinolfiLE,RagoneE,etal.Streptococcusbovis endocarditisanditsassociationwithchronicliverdisease:an underestimatedriskfactor.ClinInfectDis.2004;38:1394–400.

13.HoenB,Brianc¸onS,DelahayeF,etal.Tumorsofthecolon increasetheriskofdevelopingStreptococcusbovis endocarditis:case–controlstudy.ClinInfectDis. 1994;19:361–2.

14.TripodiM-F,FortunatoR,UtiliR,TriassiM,ZarrilliR. MolecularepidemiologyofStreptococcusboviscausing endocarditisandbacteraemiainItalianpatients.Clin MicrobiolInfect.2005;11:814–9.

15.CorredoiraJ,AlonsoMP,CoiraA,etal.Characteristicsof Streptococcusbovisendocarditisanditsdifferenceswith Streptococcusviridansendocarditis.EurJClinMicrobiol InfectDis.2008;27:285–91.

16.Fernández-RuizM,Villar-SilvaJ,Llenas-GarcíaJ,etal. Streptococcusbovisbacteraemiarevisited:clinicaland microbiologicalcorrelatesinacontemporaryseriesof59 patients.JInfect.2010;61:307–13.

17.FitzmauriceGJ,McKennaAJ,MurphyJ,McMullanR,O’Donnell ME.Streptococcusbovisbacteraemia:anevaluationofthe long-termeffectoncardiacoutcomes.GenThoracCardiovasc Surg.2014;62:142–214.

18.DamascoPV,RamosJN,CorrealJCD,etal.Infective endocarditisinRiodeJaneiro,Brazil:a5-yearexperienceat twoteachinghospitals.Infection.2014;42:835–42.

19.LamasC,RamosRG,LopesGQ,etal.BartonellaandCoxiella infectiveendocarditisinBrazil:molecularevidencefrom excisedvalvesfromacardiacsurgeryreferralcenterinRiode Janeiro,Brazil,1998to2009.IntJInfectDis.2013;17:e65–6.

20.BoleijA,vanGelderMM,SwinkelsDW,TjalsmaH.Clinical importanceofStreptococcusgallolyticusinfectionamong colorectalcancerpatients:systematicreviewand meta-analysis.ClinInfectDis.2011;53:870–8.

21.KrishnanS,EslickGD.Streptococcusbovisinfectionand colorectalneoplasia:ameta-analysis.ColorectalDis. 2014;16(9):672–80.