w w w . h t c t . c o m . b r
Hematology, Transfusion and Cell Therapy
Original article
COVID-19 in hematology: data from a hematologic and transplant unit
Marcia Garnica
a,b,∗, Marcia Rejane Valetim
a, Paulo Furtado
a,
Maria Claudia Moreira
a,b,c, Ricardo Bigni
a,c,d, Simone Vinhas
a, Paulo Cesar Dias
a, Ilza Fellows
a, Wolney Martins
a,eaComplexoHospitalardeNiterói(CHN),Niterói,RJ,Brazil
bUniversidadeFederaldoRiodeJaneiro(UFRJ),RiodeJaneiro,RJ,Brazil
cInstitutoNacionaldoCâncer(INCA),RiodeJaneiro,RJ,Brazil
dAméricaOncologia,RiodeJaneiro,RJ,Brazil
eUniversidadeFederalFluminense(UFF),Niterói,RJ,Brazil
a r t i c l e i n f o
Articlehistory:
Received8June2020 Accepted21August2020
Availableonline6September2020
Keywords:
COVID-19 SARS-CoV-2 Cancer
Stemcelltransplant Healthcareworker Pandemic
Cancercare
a bs t r a c t
DuringtheCOVID-19pandemic,specialattentionhasbeenaddressedincancercaretomit- igatetheimpactonthepatient’sprognosis.WeaddressedourpreparationtofaceCOVID-19 pandemicinaHematologicalandStemCellTransplantUnitinBrazilduringthefirsttwo monthsofCOVID-19pandemicanddescribedCOVID-19casesinpatientsandhealthcare workers(HCW).Modificationsindailyroutinesincludedaseparationofareaandprofes- sionals,SARS-CoV-2screeningprotocols,andothers.Atotalof47patientsand54HCW weretestedforCOVID-19,byPCR-SARS-CoV-2.Wereport11casesofCOVID-19inhemato- logicalpatients(including2poststemcelltransplant)and28casesinHCW.Hematological casesweremostsevereormoderateandpresentedwithseveralpoorriskfactors.Among HCW, COVID-19weremostlymild, andall recoveredwithout hospitalization.Acluster wasobservedamongHCW.Despiteadecreaseinthenumber ofprocedures,theTrans- plantProgram performed8autologousand4allogeneicSCTduring theperiod,and49 onco-hematologicalpatientswereadmittedtocontinuingtheirtreatments.Althoughwe observedahighfrequencyofCOVID-19amongpatientsandHCW,showingthatSARS-CoV- 2isdisseminatedinBrazil,hematologicalpatientsweresafelytreatedduringpandemic times.
©2020Associac¸ ˜aoBrasileiradeHematologia,HemoterapiaeTerapiaCelular.Published byElsevierEditoraLtda.ThisisanopenaccessarticleundertheCCBY-NC-NDlicense (http://creativecommons.org/licenses/by-nc-nd/4.0/).
∗ CorrespondingAuthorat:DepartmentofInternalMedicine;UniversidadeFederaldoRiodeJaneiro,RJ,Brasil E-mailaddress:marciagarnica@hucff.ufrj.br(M.Garnica).
https://doi.org/10.1016/j.htct.2020.08.004
2531-1379/©2020Associac¸ ˜aoBrasileiradeHematologia,HemoterapiaeTerapiaCelular.PublishedbyElsevierEditoraLtda.Thisisan openaccessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/).
Introduction
SincealltheworldhasbeenfacingCOVID-19pandemic,con- cernsabouthematologicalpatientshavebeenaddressed.1,2 Newdiagnosisofacuteorchronicleukemia,lymphoma,mul- tiplemyelomaisstillbeingmade,andpatientsmustgoonin theirtreatmentstomaintainresponseandprognosis.There arefewreportsabouthematologicpatientsandCOVID-19until now, but they reported more severe disease in this popu- lation.3–7 Therationaleisthat hematologiccancerconfers immunosuppressionbyitself or byits treatment, and it is already known that the development of any severe infec- tioncanmodifythetreatmentschedule,impactingprognosis.
AnotherspecialissueinCOVID-19scenarioisabouttheaccess andthequalitycareofcancertherapysincethereareover- crowdedhospitalsanddeficienciesinbloodsupplies.
COVID-19wasfirstnotedinBrazilattheendofFebruary, and a few days after, community transmission was docu- mented. In the last two months, it spread to all Brazilian regions.Brazilfacesseveredifficultyinaccessdiagnosistests forall,sotestinghasbeenusedmostlyforindividualsinrisk groupconditions,healthcareprofessionals,orpatientswho requirehospitalizations.8
Inthismanuscript,weaddressourpreparationtofacethe COVID-19pandemicduringthefirsttwomonthsanddescribe COVID-19documentedcasesinpatientsandhealthcarework- ers(HCW):fromdiagnosistooutcomes.
Methods
Thisisacaseseriesstudyfromhematologicalpatientstreated fromMarch12thtoMay21thinComplexoHospitalardeNiterói, aquaternarylevelhospital,referenceforstemcelltransplan- tation (SCT), and solid organ transplant in Rio de Janeiro, Brazil.Thestudyperiodcoincideswiththefirst2monthsafter thedocumentationofcommunitytransmissionofCOVID-19 in Brazil.The hospitalhas a SCT Program since2007 and performsamedianof100autologousand30allogeneicSCT (relatedandunrelated)peryear.Thetransplantunit(UTX)has 26HEPAfilteredsingle-roombedsandreceives patientsfor SCTandalsohematologicalpatientsforchemotherapyand immunotherapy.ADay-Clinichospitalwith15bedsalsointe- gratestheunit.Thisstudywasapprovedbytheinstitutional ethicscommittee(number30907420.1.0000.5455).
Protocolsanddatacollection
SinceWHOdeclaredCOVID-19apublichealthemergencyof international concern in January 31th, the Transplant Unit planned modificationsregardingdaily routines,inaddition tointensemodificationsinallhospital.AfterWHOdeclared COVID-19apandemic, aCOVID-19Committeewas formed to coordinate all actions and specific areas for COVID-19 patientswheredelimited,intendednottopermitcrossover of COVID-19 and other patients. Regarding the Transplant Unit,hematologystaff,transplantinfectiousdiseasesspecial- ist,andtransplantcoordinationhavegeneratedguidelinesto bestbalancetheriskofbaselinemalignancieswiththeriskof
COVID-19infectionandmortality.InternationalandNational recommendations were references for our actions, as well asreportsfromothertransplantcentersthathadpreviously facedCOVID-19.Caremodificationsincludedinpatientsand outpatients;transplantindicationtiming;bloodcellsupply;
and intensive careunit. Firstly,wefocusedon patient and familyeducation abouttheimportanceofsocialdistancing, handhygiene,andmasking.Writtenmaterialwasdistributed toall.RestrictioninpeoplecirculationinsidetheUTXhasbeen applied,andseveralmodificationswereimplementedbefore andongoingthepandemicweeks.Welimitedinpatientscare- givertoone,andvisitorsarestrictlylimited.
UTXentrancehasbeenconfinedtoasinglepoint,whereall patients,families,andHCWarescreenedregardingsymptoms andexposition.PatientswithanysymptomsregardingCOVID- 19aremaskedandtransferredtoaspecificEmergencyRoom tobetested.HCWorfamiliesthataresymptomaticarenot allowedtoentertheUnit.
Sincethebeginningoftheprogram,medicalstaffs’surveil- lanceofrespiratorysymptomswasintensifiedandtestingall symptomatichasbeenroutine.
Regardingpatientscare,alladmissionsofSCT,donorand recipient, scheduled chemotherapy,or unscheduledadmis- sions such as febrile neutropenia, and others have been clinicalandlaboratoryscreenedbySARS-CoV-2PCR.
Wegavecontinuedtrainingregardingsecure,IPE,hospital andtransplantflows,intubation,andothersforallstaff,and relevantdatahavebeensharedwithall.
Forthisanalysis,epidemiological,clinical,andlaboratory datafromCOVID-19caseswere reviewed,andthe outcome described.ForHCW,weperformedawebquestionnaire.This questionnairewasappliedtwice,with30daysapart,toiden- tifyCOVID-19cases.
Datawerereportedasfrequencies,proportions,ormedi- ans.Thechi-squaredtestwasappliedtocomparefrequencies andrates.Kaplan-Meirwasappliedtosurvivalanalyses,and curveswerecomparedbylog-rank.Wedefinedastatistically significantp-valuelowerthan0.05.
Results
SARS-CoV-2testingandscreening
Atotalof47onco-hematologicpatientsweretestedforCOVID- 19intheUnit.ThescreeningwasperformedusingSARS-CoV2 PCRforallcases.Thetestwasappliedto30symptomaticand 17asymptomaticpatients.Screenedasymptomaticpatients were:SCTdonors(n=4),SCTrecipients(n=10),hematological patientsbeforescheduledchemotherapy(n=3).Nopositive testwasnotedinasymptomaticscreening,butonlyinsymp- tomatic patients(10 cases;33% ofsymptomatic;21% ofall tested).ACOVID-19caseperformedthetestinotherhospital, butshewastransferredtoourhospitaltotreatment.
Screeningwasdonein54healthcareworkers:40symp- tomatic and 14 asymptomatic justified by exposure to SARS-CoV-2.OnlysymptomaticHCWtestedpositive(28cases;
70% ofsymptomatic,52%oftested).FrequenciesofCOVID- 19intestedandsymptomaticHCWwerehighercomparedto
A
COVID-19 acquisition: community (blue cases) and intrahospital (red cases)
B
0 1 2 3 4 5 6
10-Mar 20-Mar 30-Mar 9-Apr 19-Apr 29-Apr 9-May 19-May
0 1 2 3 4 5 6
10-Mar 20-Mar 30-Mar 9-Apr 19-Apr 29-Apr 9-May 19-May
Fig.1–TimelineofCOVID-19casesinhematologicalpatients(Fig-1A)andinhealthcareworkers(HCW)(Fig-1B)fromSCT Unit.COVID-19acquisition:community(bluecases)andintra-hospital(redcases).
1,0
0,8
0,6
Cumulative incidence
0,4
0,2
0,0
1,0
Physicians RN Others 0,8
0,6
0,4
0,2
0,0
,00 20,00 40,00 60,00 ,00 20,00 40,00 60,00
Fig.2–CumulativeCOVID-19incidenceinhealthcareworkers(HCW)(Fig.2.1)andbyprofessionalcategories(Fig.2.2).
hematologicalpatients(52%vs.21%;p=0.003and70%vs.33%;
p=0.005;respectively).
COVID-19casesinhematologicalandtransplantpatients
Eleven onco-hematological patients were diagnosed with COVID-19,includingtworecipientsofhaploidenticalstemcell transplant(bothlatephasepost SCT- afterD+100),and 9 patientswithonco-hematologicalmalignancies.Clinicaland laboratorydataareshowninTable1.
Regarding haploidentical patients, they were treating chronic severe GVHD at the moment of COVID-19, and immunosuppression included corticosteroids. Regarding onco-hematologicalpatients,twoepisodesofCOVID-19were noted in untreated newly diagnosed patients. Most cases
SP 75.000
70.000 65.000 60.000 55.000 50.000 45.000 40.000 35.000 30.000 25.000 20.000
Notifications
Accumulated cases
15.000 10.000 5.000 0
27/0202/0305/0309/0313/0317/0321/0325/0329/0302/0406/0410/0414/0418/0422/0426/0430/0404/0508/0512/0516/0520/05 RJ ES MG
Fig.3–CumulativecasesofCOVID-19insouth-eastern StatesinBrazilduringpandemic.SP:SãoPauloState;RJ:
RiodeJaneiroState;ES:EspíritoSantoState;MG:Minas GeraisState.
Source:https://covid.saude.gov.br9
Table1–Characteristicsofhematologicalpatientswith COVID-19.
Characteristics n=11(%)
Age,median[range](years) 41(3–83)
Male,n(%) 6(55)
Baselinedisease,n(%)
o Acutemyeloidleukemia 3(27)
o AcuteLymphoidleukemia 3(27)
o Myelodysplasia 1(9)
o MultipleMyeloma 1(9)
o HodgkinDisease 1(9)
o Non-HodgkinLymphoma 2(18)
PreviousSCT,n(%)
o AutologousSCT 0
o HaploidenticalAllogeneicSCT 2(18) Treatmentphase,n(%)
o Beforefirst-linetherapy 2(18)
o Induction/first-linetherapy 4(36)
o Intensification/Consolidation 3(27)
o Postallogeneicstemcelltransplant 2(18) COVID-19symptoms,n(%)
o Fever 9(82)
o Cough 7(64)
o Dyspnea 5(45)
o Asthenia 5(45)
o Muscleache,asthenia 2(18)
o Gastrointestinalsymptoms 2(18)
o Headacheordizziness 1(9)
o Upperrespiratorysymptoms 1(9)
COVID-19staging,n(%)
o Mild 2(18)
o Moderate 5(45)
o Severe 4(36)
Comorbidities,n(%)
o Ageover60y 3(27)
o Cardiologicaldisease 2(18)
o Diabetes 3(27)
o ChronicRenalFailure 1(9)
o Obesity 1(9)
–Table1(Continued)
Characteristics n=11(%)
o Otherimmunosuppression 0
o Morethan2comorbidities 4(36) LaboratorialfindingsduringCOVID-19
o Neutrophil,cells/mm3,median(range) 803(<100–13,691) o Neutropenia(neutrophils<500cells/mm3),
n(%)
5(45%)
o Lymphocytes,cells/mm3,median(range) 503(<100–2312) o Lymphopenia(totallymphocytes
<1000cels/mm3),n(%)
8(73)
o SevereLymphopenia(<200cells/mm3),n (%)
5(45)
o Creactiveprotein,mg/dLmedian(range) 18.62(0.14–69) o D-dimerlevel,mcg/dLmedian(n=8) 2.56(0.59–7.9) o D-dimer>3mcg/dL,n(%) 2
o Venouslactate,mg/dLmedian(n=7) 29(14–38) o Venouslactate>20mg/dL,n(%) 5
o Fibrinogen,mg/dLmedian(n=4) 630(527–943) o Troponin,ng/dLmedian(n=7) 46(<5–1099) o Ferritin,median(n=6) 1,215(189–4957) LungCTscan,n=9(%)
o Limitedground-glassopacity(<50%) 2(22) o Limitedground-glassopacity(>50%) 4(44) o Diffuseground-glassopacity 3(33) Complications,n(%)
o Hospitalization 10(83)
o Intensivecare 6(55)
o SARS 4(36)
o Hemodynamicinstability 5(45)
o Hemodialysis 2(18)
o Thromboembolisms 1(9)
Outcome,n(%)
o Recovered 5(45)
o Ongoing 1(10)
o Dead 5(45)
*01 patient with severe disease had chronic renal disease in hemodialysis.
SCT:Stemcelltransplantation;CT:Computedtomography.
weremoderateorsevere(n=9;82%),and5(45%)dieddueto COVID-19.Onepatientisstillontreatment,butrecovering.
COVID-19casesinHCWfromtransplantunit
Data from 84HCW were collected,including 37 physicians and18registerednurses(RN).Itrepresents100%ofphysicians andRNwhoworksintheSCTUnit,asroutineorconsulting physicians.Forty-six(55%)HCWhaveemploymentinmore than one hospital, and 37 (44%) work atleast 4 days per weekintheUTX.Fifty-fourHCWperformedatleastonetest duringthestudy.COVID-19weredocumentedin28(33%)of HCW:21.6% ofphysiciansand 44.4% ofRN. All HCW were symptomatic,but thediseaseintensitywasmildormoder- ate.Nohospitalizationwasrequired,andallHCWrecovered.
FrequencyofCOVID-19inHCWwho worksinanotherhos- pital (46% vs. 60%; p=0.21) or works at least 4 days per week(50% vs. 39%;p=0.36) were not different from those whoworkonlyinourhospitalorfewdaysperweekinthe UTX.
TimelineofCOVID-19inonco-hematologicalpatientsand HCW
The timeline of COVID-19 cases is represented in Fig. 1A.
Our first case of COVID-19 in hematological patients was documented on March 30th, in another hospital, and the number ofcases increasedafter April 15th. Three patients developedCOVIDduringhospitalization,butintwo,aclose relativewas the probablesource ofinfection. In the other patient,thesourcecouldbeintrahospital.Inallthe others, COVID-19symptomswerepresentathospitalization,andthe patientwastreatedoutsideUTX.RegardingHCW,COVID-19 cases started earlier comparing to hematological patients, but most HCW cases occurred after the second week of April,withaclusterdistributionofthirteencasesin2weeks.
(Fig.1B)Afterthiscluster,trainingandscreeningwereinten- sified,and universal use ofmasks duringall hospitalstay, includingHCWcommonareas,wasthenimplemented.HCW casesstilloccurred butin moreregular distribution during weeks.Fig.2.1showsthecumulativeincidenceofCOVID-19 inHCW,andFig.2.2,theincidencebyprofessionalcategories (p=0.13).
The spread in number of COVID-19 in hematological patientsand inHCW aftersecond weekofApril issimilar tocasesdistributioninRiodeJaneiroStateduringthesame period(Fig.3).
TransplantprogramandproductiononUTX
During the same two months, a total of 61 hematolog- ical patients were admitted in the UTX. Autologous and allogeneic SCT was performed in eight and four patients, respectively.Despite twoautologouspatients(admissionin UTXoccurredbeforethedocumentationofcommunitytrans- mission inBrazil), allrecipients and donorswere screened by SARS-CoV-2 PCR before admission or stem cell har- vest. No COVID-19 was observed in SCT during the early phase.
Discussion
OurexperienceduringtheinitialmonthsofCOVID-19pan- demichighlightedsomeobservations:COVID-19presentsas moderateorseverecasesinonco-hematologicalpatients,and themortalitywashigh.Highintensivelytreatedpatientsor thosewithcomorbiditieswereatworseriskforsevereCOVID.
AlargeproportionofHCWexperiencedCOVID-19,indepen- dently ofthecategoryofprofessionals.Wecould observea clusterofCOVID-19inHCW,suggestingpossibletransmission withinHCW.Afterintensifiedmeasures,thespreadofcases inpatientsand HCWwere similartothosereportedinour State,andtheUnitwasmaintainedasa“COVID-19freezone”.
Regardlessofthepandemic,thetransplantprogramwascon- tinued but had a 50% reductionin autologous transplants procedures. Regarding allogeneic, we did not experience a reductionintransplantsprocedures.Thisworkforcepriories theimportanceofkeepcancertreatmentgoing,andsomiti- gatetheimpactofpostponingSCTinhighriskcancerpatients.
TheknowledgeofCOVID-19isinprogression.Thedisease wasfirstdocumentedafewmonthsagobutisnowspreading worldwide.Descriptionofmanifestationsandoutcomesfrom specificsub-settingsofpatientsisamandatoryissueforabet- terunderstanding ofthisnewpathologyand providestools tofaceit.10–13Fewreportsaddressedhematologicalpatients.
DatafromChinaandFrancereportedconcerningoutcomes:
85%and40%mortalityratesamonghematologicalpatients, respectively.3,4Mostpatientshadothercomorbiditiesdespite hematological cancer,andthe COVID-19manifestationwas frequentlysevere,requiringmechanicalventilationandinten- sivecareinahighproportionofcasesfrombothseries.Data fromItaly,includingsolidtumorpatients,showedbetterout- comesthanChinaandFranceseries,butallauthorsconcluded thatCOVID-19hasaworseevolutionincancerpatientscom- paredtonon-cancerpopulation.5,6Inourseries,themortality ratewassimilartoFrancereports.Wealsofindpoorlabora- torymarkersandseverepulmonaryinvolvementattheonset ofseverediseases.
Ontheotherhand,mildandmoderatecasesatonsethad uncomplicatedevolution.Itisimportanttoaddressthattheir andourcaseswereallsymptomaticpatientsthathadadoc- umented COVID-19.Itisacrucialbiassinceasymptomatic oroligosymptomaticcasesarenotdocumentedunlessthey require medicalassistanceorhospitalization forother rea- sons.Thereisapossibleoverestimationofcomplicationsand mortalityrates.
Regarding HCW,wereportahighincidenceofCOVID-19 regardlessoftheprofessionalcategory,andwewereunable toestablishanassociationwithworkcharacteristicssuchas frequencyandworkinmorethan onehospital.HCWcases increasedconcomitantlywithcasesinourState,butwecould observeaclusteratthebeginningoftransmission.Thisfact suggeststhatapossibletransmissionwithinHCWhappened, asallCOVID-19onco-hematologicalpatientsweremanaged outsidetheUTX,andnocaseinthehospitalizedpatientwas identifiedinthesameperiod.TheCOVID-19rateinHCWwas higherthan somereportsfromItaly,5,14 butsimilartofirst reports from China. 15 Cluster distribution was also noted inSingaporeandChina.16,17 HCWisconsideredahigh-risk
groupforinfection and transmission, but fortunatelymost casesweremild.18
ThishighincidenceofCOVID-19inHCWhighlightedthe importanceofintensescreening,regular training,and ade- quatepersonalprotectiveequipmenttolimitthespreadand toreducetheriskforHCWtobecomeinfected.Anysymptoms orsuspectedcommunityexpositionshouldbemanagedasa possiblecase,andtheHCWmustberemovedfromworkuntil appropriatedocumentation.Thefrequencyoftestingpositive was70%insymptomaticHCW,averyhighproportioncom- paredtosymptomaticonco-hematologicpatients.Although, wedidnotfind COVID-19documentationinasymptomatic HCW, pre-symptomatic transmission is of great concern.
Impact of asymptomatic HCW screening is not clear, but measurestoreducepre-symptomatictransmissionmustbe implemented.16
Despite the pandemic, transplant programs from other countriesmaintainedtheprogramactive,aspostponingtrans- plantationisnotfeasible insomescenarios.TheEuropean Society for Blood Marrow Transplantation (EBMT)and The BrazilianSocietyforBloodMarrowTransplantation(SBTMO) recommendationsallowproceduresifthepatients’safetyis maintained.19,20Wedecidedtomaintaintheprogramactive but limited theprocedure to those inwhich the prognosis wouldbeimpactedbypostponingtransplantation.Thisdeci- sionwasbasedonanintensecollaborationoftheinstitution asawholeandrevisedwithdailyresults.10,21
Asia,Europe,andNorth Americaare inadifferentpan- demicphasecomparedtoBrazil.Theseregionsarereopening, butBrazilhasnotachievedthepeakofincidenceyetandhas anincreasingnumberofinfectedanddeathsdaily.Unfortu- nately,alltheworldisexposedtosecondormorewavesof COVID-19,untilanefficientvaccineisavailable.SARS-CoV-2 willremainaconcernforalongtime.Wehopeourexperience maycontributetoabettercomprehensionofthediseasein theonco-hematologicalscenarioandimprovethecapacityto mitigatethenegativeimpactincancercareassistanceduring thePandemic.
Conflict of Interest
Theauthordeclaresnoconflictsofinterest.
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