Chronic pulmonary aspergillosis: A frequent and potentially severe disease

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Médecineetmaladiesinfectieuses45(2015)128–132

Original article

Chronic pulmonary aspergillosis: A frequent and potentially severe disease

L’aspergillose pulmonaire chronique : une pathologie fréquente et potentiellement grave

H. Benjelloun

^a^,∗

, N. Zaghba

^a

, N. Yassine

^b

, A. Bakhatar

^a

, M. Karkouri

^b

, M. Ridai

^c

, A. Bahlaoui

^b

aServicedesmaladiesrespiratoires,hôpitalIbnRochd,Casablanca,Morocco

bServiced’anatomiepathologique,hôpitalIbnRochd,Casablanca,Morocco

cServicedechirurgiethoracique,hôpitalIbnRochd,Casablanca,Morocco Received5November2014;receivedinrevisedform6January2015;accepted29January2015

Availableonline18February2015

Abstract

Introduction.–Chronicpulmonaryaspergillosisisapulmonaryfungalinfectionwithvariouspresentationsthatcanoccuronapre-existingcavity, oftenasequeloftuberculosis.Theobjectiveofourstudywastoreportthediagnosticandtherapeuticmanagementofpulmonaryaspergillomain ourstructure.

Patientsandmethods.–Weretrospectivelystudied81casesofpulmonaryaspergillomahavingoccurredintherespiratorydiseasesunitofthe CasablancaIbnRochdhospital,over11years.

Results. –Weincluded48maleand 33femalenon-immunocompromisedpatients,withanaverageageof 51years(27–75).Ahistoryof tuberculosiswasrecordedin78cases.Hemoptysiswastherevealingsymptomin73cases.Acharacteristic“bell-like”imagewasobservedin25 cases.Theserologicalresultswerepositiveforaspergillusin54cases.Thetreatmentwassurgicalin50casesandmedicalin24cases.Fivepatients died.

Discussion. –Asignificantnumberofpulmonaryaspergillomacases wererecordedinourstudy,occurringmostfrequentlyonsequelsof tuberculosis.Thisdiseaseiscurrentlycommonincountrieshighlyendemicfortuberculosis;earlyandadequatemanagementisrequired.

Conclusion.–Aspergillosisisafrequentandpotentiallyseverediseaseoccurringonpre-existinglesions,mostofteninourcontextsequels oftuberculosis.Surgicalresectionisthereferencetreatmentbutisthecauseofasignificantmorbidityandmortality.Preventivemeasuresare mandatory.

Keywords: Aspergilloma;Mycosis;Sequeloftuberculosis;Hemoptysis Résumé

Introduction.–L’aspergillosepulmonairechroniqueestuneinfectionmycosiquepulmonairequipeutprendredifférentsaspectsetsurvenirsur unecavitépréexistante,leplussouventséquellaired’unetuberculose.L’objectifdecetravailestderapporterlapriseenchargediagnostiqueet thérapeutiquedesaspergillomespulmonaireschezdespatientsnonimmunodéprimésdansnotrestructure.

Patientsetméthodes.–Nousrapportonsuneétuderétrospectiveportantsur81casd’aspergillomepulmonairecolligésauservicedesmaladies respiratoiresducentrehospitalieruniversitaireIbnRochddeCasablanca,surunepériodede11ans.

Résultats. –Il s’agissaitde48hommeset33femmesnon immunodéprimés.Lamoyenne d’âgeétait de51ans(27–75). L’antécédentde tuberculoseétaitnotédans78cas.L’hémoptysieétaitlesymptômerévélateurdans73cas.L’imagecaractéristiqueengrelotétaitrelevéedans 25cas.Lasérologieaspergillaireétaitpositivedans54cas.Letraitementétaitchirurgicaldans50casetmédicaldans24cas.Cinqdécèsétaient rapportés.

Discussion.–Àtraverscetteétude,unnombreimportantd’aspergillomepulmonaireétaitrecensé,survenantpourlaplupartsurdesséquelles detuberculose.Cetteaffectionest,àcejour,fréquentedanslespaysàforteendémietuberculeused’oùlanécessitéd’unepriseenchargeprécoce etbienadaptée.

∗Correspondingauthor.

E-mailaddress:hananebenj@yahoo.fr(H.Benjelloun).

http://dx.doi.org/10.1016/j.medmal.2015.01.014

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Conclusion.–Lagreffeaspergillaireestunepathologiefréquenteetpotentiellementgravesurvenantsurdeslésionspréexistantesleplussouvent tuberculeuse.Lachirurgied’exérèsedemeurelathérapeutiquederéférencemaislacaused’unemorbimortaliténonnégligeable.Lesmesures préventivesrestentindispensables.

Motsclés:Aspergillome;Mycose;Séquellesdetuberculose;Hémoptysie

1. Introduction

Pulmonary aspergillosis is an opportunistic pulmonary mycosis pulmonary fungal infection with various presenta- tionsdependingontheunderlyingcondition andthe patient’s immune status. Pulmonary aspergilloma is the development ofAspergillushyphaeinpre-existingcavities,usuallysequels of tuberculosis [1–3]. It can present as simple pulmonary aspergilloma or chronic cavitary pulmonary aspergillosis (CCPA)[4].Surgicalresectionistheonlytrulycurativetreat- ment and should be planned as soon as possible to prevent sometimes-fatalinfectiousandhemorrhagiccomplications.The severityofthediseaseisrelatedtoitsmorbidityandmortality [5].Theobjectiveofthisstudyistodescribetheepidemiological, clinical,diagnosticandtreatmentofthisfungus.

2. Patientsandmethods

Weconductedaretrospectivedescriptivestudyof81casesof pulmonaryaspergillomacollectedfromAugust2003toSeptem- ber 2014, in the respiratory diseases unit, at the Casablanca Ibn Rochd Teaching hospital. We selected the records of allHIV-negativenon-immunocompromisedpatientswhowere diagnosedwithpulmonaryaspergillomaaccordingtoradiolog- ical,clinical,and/orbiological,and/orhistologicaldata.

Aninformationsheetwasstudiedforeachpatient.Itincluded epidemiological(age,gender),clinical(underlyingconditionor clinicalhistory),andlaboratory(chestimaging,bronchoscopy, aspergillusserology)data.Thehospitalmorbidityandmortality, aswellastheshortandlong-termoutcomewerealsoconsidered.

Thedefinitionofaspergillusinfectionisnotclearlydefined and many entities have been described with various names.

TheclassificationoftheInfectiousDiseasesSocietyofAmer- ica(IDSA)distinguishessimplepulmonaryaspergilloma(SPA) fromchronicpulmonaryaspergillosis(CPA)[6].

The latter is classified as: chronic cavitary pulmonary aspergillosis (CCPA), former complex aspergilloma; chronic necrotizing pulmonary aspergillosis (CNPA); and chronic fibrosingpulmonaryaspergillosis (CFPA),withspecificdiag- nosticcriteria.

This classification divides aspergilloma into 2 categories:

SPA and CCPA. [6] SPA is a parenchymal cavity with well definededgesevolvingwithoutassociatedpleuralparenchymal abnormalities[2].CCPAisdefinedastheoccurrenceofmultiple cavities that may or may not contain an aspergilloma, asso- ciatedwithpulmonary andsystemic symptoms, andelevated inflammatorymarkers[6–8].

Table1

Clinicalpresentationofpulmonaryaspergillomacases.

Présentationcliniquedescasd’aspergillomespulmonaires.

Number Percentage(%)

Historyoftuberculosis 78 96.3

Delaybetweenonsetoftuberculosis andaspergillosis

2–10 32 39.5

10–20 43 53.1

20–23 6 7.4

Hemoptysis 73 90

Dyspnea 56 69.1

Chronicbronchorrhea 27 33.3

Thoracicpain 30 37

Wasting 19 23.4

Fever 12 14.8

OurseriesisanillustrationandadescriptionofAPCCina non-immunocompromisedpopulationwithahighprevalenceof tuberculosis.

3. Results

Forty-eight male and 33 female patients were diagnosed withpulmonaryaspergillomaduringthestudyperiod.Theaver- ageagewas51years(27to75years).Seventy-eight(96.3%) patients hadahistoryof treatedpulmonarytuberculosis. The averagedelaybetweentheonsetoftuberculosisandaspergillo- siswas12.87years(2to23years).Eighteen(22.2%)patients were smokersand4 of thesepresented withchronicobstruc- tivepulmonarydisease(COPD),and4(5%)patientspresented withwell-controlled non-insulindependentdiabetes.Noshort or long-term oral or inhaled corticosteroid therapy was doc- umented. The reasons for consulting were: hemoptysisin 73 (90%)cases(Table1),withanaveragedelaysincetheonsetof symptomsof3months(2daysto7months).Theclinicalexami- nationrevealedaretractedhemithoraxin11(13.6%),stertorous breathing in 72 (89%) patients, andwheezing in28 (34.5%) patients.

Thoracicimaging(Table2),including X-raysandCTscan performed in every cases, revealed pleural thickening in 38 (47%)patients,cavitaryimagein26(32%)patients,andachar- acteristic “bell-like”imagein25 (31%) patients.The lesions werepredominantintheupperlobes,74(91.3%)patients.

Laboratorytestsresultsrevealedanacceleratedsedimenta- tionratein28(34.5%)patients,hypochromicmicrocyticanemia in17(21%)patientswitharangeof6.4to11.1g/dL,andleuko- cytosiswithapredominanceofPNNin13(16%)patientswith

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Table2

Thoracicimagingofpulmonaryaspergilloma.

Imageriethoraciquedesaspergillomespulmonaires.

Pleuralthickening 38 47

Imageofcavities 26 32.1

“Bell-like”image 25 30.8

Lungnecrosis 23 28.4

Uncomplicatedpulmonaryaspergilloma 8 9.8 Chronicpulmonaryaspergilloma 73 90.2

Superiorlobes 74

Rightside 62 91.3

Imageofcavities 26 76.5

arangeof9,700to14,500cells/mm³,withoutneutropenia,controlled by the prescription of empiric antibiotic therapy. The cytobacteriologicaldirectexaminationofsputum,performedin 15(18.5%)patients,wasnegative.Aflexiblebronchoscopy,per- formedinallourpatients,revealedendobronchial bleedingin 20(24.7%)patients,aspergillosismycetomain4(5%)patients, abronchialinflammatoryconditionin45(55.5%)patients,and wassubstantiallynormalin5(6%)patients.Aspergillusfumi- gatuswasisolatedinthebronchialaspirateof9(11%)patients.

Screening for the Koch bacillus by direct examination and cultureofsputumandbronchialaspiratewasnegativeinevery case.TheHIVserologywasnegativeineverycase,aswellas thehydatidserologyperformedin8(9.8%)patients,allingood condition,fromruralareas,presentingwithhistologicallycon- firmedSPA.Theaspergillusserologyperformedinallpatients was positivein 54(66.6%)cases. It was performed withthe immuno-electrophoresistechnique(IEP)in62(76.5%)patients, withapositivethreshold>3precipitationarcs,andwiththepas- sivehemagglutinationtechniqueintheremainingpatients,with apositivethreshold>1/320.

Thediagnosisofpulmonaryaspergillomawasmadeforall patients according toradiological aspect, association of sug- gestiveradiologicalsignsandserologypositiveforAspergillus, mycological samples, or postoperative histological findings, after ruling out some differential diagnoses mimicking pulmonary aspergilloma, including ruptured pulmonary hydatid cyst,atubercularcaseousfocus, atypicalmycobacteriosis,an excavatedlungtumor,etc.(Table3).

Thetreatmentwassurgeryin50(61.7%)cases;lobectomy wasperformedin27(54%)cases,pneumonectomyin13(26%) cases,segmentectomyin8(16%)cases,andcavernostomyin2 (4%)cases.

Table3

Elementsofpositivediagnosisofpulmonaryaspergilloma.

Élémentsdudiagnosticpositifdesaspergillomespulmonaires.

Typical“Bell-like”image 25 30.8

SerologypositiveforAspergillus fumigatus

54 66.6

IsolationofAspergillusfumigatusin bronchialaspirationfluid

9 11

Histology 50 61.7

Anexclusivelymedicaltreatmentbasedonitraconazolewas prescribed in24(29.6%)patientspresentingwithCPAforan averageof7months.Thistherapywasrecommendedforinop- erablepatients (severely alteredlungand/orcardiac function, and/orextentoflesions).Sevenpatientsrefusedanytreatment afterhemoptysiswasstoppedandwerelosttofollow-up.

TheaspergillusinfectionwasclassifiedasSPAin8(9.8%) patients,2 ofthesewerediabetic,theclinicalsymptomswere mild,thetreatment wasexclusivelysurgical,andtheoutcome was good withno recurrenceof hemoptysisafter an average follow-upof 2 yearsand4 months.Aspergillosiswas ranked CPAinotherpatientswhoseclinicalsymptomsweremoresevere and42(57.5%)patientsunderwentsurgery.

ThepostoperativeoutcomeofpatientspresentingwithCCPA, formerly knownas complexaspergilloma,was good,withno recurrenceofhemoptysisin35(83.3%)cases,includingfor2 diabetic patients, afteran averagefollow-upof4 yearsand2 months.Fourpatientspresentedwithrecurrenceofhemoptysis after6to24postoperativemonthsandadiagnosisofbacterial superinfectionoftuberculosissequelswasmade.Threepatients diedpostoperatively,allpresentingwithCOPDandCCPA.

The outcome ofpatients treatedwithantifungalsonlywas marked by the recurrence of hemoptysis in 12 (50%) cases.

This couldbe explainedby theunavailability oftreatment in ourcontextandthe extentoflesions.Twopatients presenting withnon-operatedCPAdiedfromsuddenhemoptysis.

4. Discussion

Aspergillosisisoneofthemostfrequentopportunisticpul- monarymycoses. Theintracavitaryaspergillomaisbyfar the mostcommonpresentation.Aspergillusfumigatusisthespecies mostoftenimplicatedinhumandisease,intemperatecountries.

Itisresponsiblefor80to90%ofpulmonaryaspergillosiscases [1,2,9,10].

Histologically,theaspergillomaisasaprophyticproliferation ofaspergillussporesorganizedasinadensemycelialfelting,or

“mycetoma”withinapreformedcavity[9,11,12]thatisoftena sequeloftuberculosis[3,8,13–15].

Thisinfectionwasobservedin96.3%ofourpatients.This rate is comparable to the literature data, 71.1% of cases as reportedbyChenetal.[15],79.4%byZaitetal.[2],oreven 100%byAdeetal.[5].

Conversely, 11to17% ofpost-tuberculouscavities canbe complicated by aspergilloma [7,12,16].This highpercentage couldbeexplainedinourstudybythesusceptibilityofyoung Moroccanmalepatientstotuberculosisinfection.Thisdiseaseis stillcommoninareasofhighTBendemicitywherethepandemic HIVinfectionhelpedtoincreasethespreadofthisdisease.

However,anyparenchymalcavityislikelytobecomplicated byaspergillosis,includingbronchiectasis,bullousemphysema, andsarcoidosis.Otherconditionsmayalsobecomplicatedby aspergillosis such as pneumoconiosis, fibrosis of ankylosing spondylitis or scleroderma, excavated lung cancer, bacterio- logicallysterilizedlungabscess,pulmonaryinfarctionsequels, cysts,sequesters[2,3,8,10,16–19].

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Pasquieretal.reportedacaseofpulmonaryaspergillomain apatientpresentingwithseverethalassemia[19].Hemoptysis remainsthehallmarkofpulmonaryaspergillomaandisreported in50to95%ofcases,accordingtotheauthors[8,9,14,15,20,21].

Thisiswhatwasobservedinourserieswhere90%ofour patients consulted for hemoptysis.That said,the recruitment ofpatientsinourpneumologydepartmentprobablyexplainthe highrateofhemoptysisrevealingtheaspergillusinfection.This infectionisoftenrecurrent,sometimesabundant,andlifethreat- ening[7,20].Othernonspecificsignsmaybeobservedsuchas cough, sputum,chest pain, anddyspnea [3,22].Chronic pul- monaryorsystemicsymptomslastingformorethan3months suggestCPA[4,8].Theaspergillomaisdiscoveredduringsys- tematicX-rayscreeningin10to30%of cases[9].ChestCT isthefirst-lineexaminationforthepositivetopographicdiagno- sis,tolookforotherlocations,andthemonitoringoflesions[9].

ItalsoallowsdiscriminatingbetweenSPAandCPAor CCPA [1,3,9,22–24].Thecharacteristicimageisacavitycontaining a rounded or oval mass, well defined, dense, and homoge- neous,declive, andmobile, whichmay containcalcifications [3,9,11,13,14]. The surrounding pleura is thickenedand may bethe earliestsign[6].Whenthemycelial massislarge, the

“meniscussign”canbe observed. Whenthe massissmall, a

“bell-like”imagecanbeobserved,typicaloftheaspergilloma.

Otheratypicalaspectsmaybeobservedleadingtomisdiagnosis as lungabscess,cavitarycarcinoma,or rupturedhydatidcyst [3,7,11,25,26].

The aspergilloma is usually located in the upper lobes [7,8,14],asreportedbyMimounietal.[27]in79.1%ofcases andinourstudyin91.3%ofcases.Thecharacteristic“bell-like”

imagewasobservedinrespectively66% and30.8%of cases comparedtoonly12.8%asreportedbyZaitetal.[2].Thispref- erentialtopographyisrelatedtotuberculosisthatusuallyaffects theupperlobes[9,22].Theaspergillomaisoftenunique,some- timesmultifocalandbilateral[9,27].Bronchoscopyisrequired.

Itallows:rulingoutsomedifferentialdiagnoses,includinglung tumors;locatingthesourceofbleeding;visualizeanaspergillus mycetoma,performingmycologicalandhistologicalsamplings for diagnostic purposes. Some authors haveeven used it for therapeuticpurposes,asfortheintrabronchialadministrationof amphotericin[28].Serodiagnosisisakeycontributorforthepos- itivediagnosisofaspergilloma[8].Italloweddiagnosing66.6%

ofpatientsinourseries,apercentageclosetothe63%reported byCaidietal.[21]andslightlylowerthanthe75.86%reported byalAde.[5].

However,serologymaybefalselynegativein5 to10% of cases,duetothedeathofthefungus, toaluminalbloodclot, tocasesof aspergillomarelatedtootherfungi,incaseof corticosteroid therapy, or to dysfunction of the T cell response inimmunocompromised patients[21,29,30].Thedetectionof serumgalactomannanantigenhasagoodsensitivityfortheearly detection of invasive aspergillosis, especially in hematologi- calmalignancies[6].Theisolation ofAspergillusoniterative samples (sputum, endobronchial aspiration) is an additional but inconstant argument for the diagnosis in 50% of cases [5].

Thepathologicalexaminationofthesurgicalspecimenmay helpcorrectthepreoperativediagnosisandprovethediagnosis formostpatients[5].

Finally, the diagnosis of pulmonaryaspergilloma is based on a setof clinical, radiological, endoscopic, biological,and possiblyhistologicalelements[17].Theoutcomemaybeaspon- taneous resolutionin7 to10% of cases, or stabilizewithout complicationsin 25%of cases[9,16,20].However, theprog- nosis remains severe given the high risk of bleeding, which canbeexplainedbylocalinvasionofthecavity’sparietalves- sels, mechanical irritation of vascularization exposed in the cavity, the presence of hemolyticendotoxins released by the fungus, or the alleged superimposedacute bacterial infection [3,31].The deathrate attributedtohemoptysisrangesfrom2 to14%or30% dependingontheseries[20].In patientswith specific risks, chronic lung superinfection may lead to local parenchymal necrosis, hence the term of chronic necrotizing aspergillosisorsemi-invasiveaspergillosis[2,17,25].Thetreat- mentofaspergillomaiscontroversialandnon-consensual[3,15].

TheIDSArecommendsasthefirstindicationeithernotreatment or surgical resection,incase of SPA [6].According tosome authors,althoughitisgenerallyacceptedthatitistechnically difficult[7],surgicaltreatmentisconsideredasstandardofcare incaseofpersistenthemoptysisortopreventseriousinfectious and hemorrhagic complications [6,9,16,31–33]. Conservative surgerywitha minimally invasive approachcanbe proposed for simplesmallaspergilloma withaperipherallocationwith betterpostoperativeresults[1,15,20].

However,accordingtotheauthorsofnumerousretrospective surgicalseries,surgerycomeswithasignificantmortalityand morbidity[3,34,35].Threedeathswerereportedpostoperatively inourseries.

Cavernostomycombined withthoracoplastycould be proposed. However, this technique remains controversial and requiresmoretesting[1,3,15,36].Bronchialarteryembolization allowsimmediatelytreatingseverehemoptysismostofthetime, andpreparingthepatientforapossiblesurgery[1,7,21,31].

In complex presentations or CCPA, short-term antifungal therapywouldbethebesttreatmentaccordingtotheIDSA,given the impaired immune status and the operative complications often associated [6].Nevertheless, someteams suggestusing plannedsurgerywithausualapproach.

Asystemicantifungaltherapy[9,15,34,35],orbyCTscan guidedintracavitaryinjections [1,21,31],does notseemtobe sufficientlyeffectiveforthisindication,intermsofradiological improvement,mycologicalsterilization,orcontrolofhemopty- sis.However,thesystemicuseofantifungalswassuggestedin therecommendationsofexpertstotreatcomplexaspergilloma, perioperativelyorexclusivelyforinoperablepatients [6,9,20].

Antifungal chemotherapy with itraconazole, voriconazole,or possiblyposaconazole,offerspotentialtherapeuticbenefitswith relatively minimal risk [6,37]. Their action remains undoc- umented for SPA, itraconazole having a better intracavitary distribution[6].Radiationtherapyhasalsogivengoodresultsas alastresortforpatientswiththreateninghemoptysisormultiple locations[1].

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5. Conclusion

Pulmonaryaspergillosisis aseveremycosisbecause ofits life-threatening bleeding complications. It grows more fre- quentlyinacavitysequeloftuberculosis,afrequentinfection incountrieswithahightuberculosisendemic.Thisstressesthe importanceofpreventionandofanearlyandadequatemanage- mentofallTBcases.

Contributionofauthors

H. Benjelloun: study design and implementation, data processingandanalysis,draftingofthearticle.

N.Zaghba,N.Yassine,A.Bakhatar,M.Karkouri,M.Ridai, A.Bahlaoui:finalapprovalofthesubmission.

N.Yassine:criticalproofreadingleadingtosignificantmod- ifications.

Disclosureofinterest

The authorsdeclare that theyhave noconflictsof interest concerningthisarticle.

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