Recommendations for interventional pulmonology during COVID-19 outbreak

(1)

www.journalpulmonology.org

SPECIAL

ARTICLE

Recommendations

for

interventional

pulmonology

during

COVID-19

outbreak:

a

consensus

statement

from

the

Portuguese

Pulmonology

Society

F. Guedes

a,b,c,∗

_,

_J.P.

_Boléo-Tomé

d

_,

_L.V.

_Rodrigues

e,f

_,

_H.N.

_Bastos

g,h,i

_,

_S.

_Campainha

j

_,

Q4

M. de

Santis

k

_,

_L.

_Mota

l

_,

_A.

_Bugalho

m,n

a_Centro_Hospitalar_do_Porto_(CHP),_Hospital_Geral_de_Santo_António_(HGSA),_Unidade_de_Broncologia,_Servic_¸o_de_Pneumologia,

Porto,Portugal

Q5

b_Departamento_de_Clínicas_{Veterinárias,}_Instituto_de_Ciências_Biomédicas_de_Abel_Salazar_(ICBAS),_Universidade_do_Porto_(UP), Porto,Portugal

c_Centro_de_Estudos_de_Ciência_Animal_(CECA),_Instituto_de_Ciências,_Tecnologias_e_Agroambiente_(ICETA)_da_Universidade_do Porto,Prac¸aGomesTeixeira,Apartado55142,4051-401,Porto,Portugal

d_Pulmonology_Department,_Hospital_Prof._Doutor_Fernando_Fonseca,_Amadora,_Portugal

e_Pulmonology_Department,_Hospital_Sousa_Martins,_Unidade_Local_de_Saúde_da_Guarda,_Guarda,_Portugal f_Faculty_of_Health_Sciences,_University_of_Beira_Interior,_Covilhã,_Portugal

g_Department_of_Pneumology,_Centro_Hospitalar_São_João,_Porto,_Portugal h_Faculty_of_Medicine,_University_of_Porto,_Porto,_Portugal

i_IBMC/i3S_-_Instituto_de_Biologia_Molecular_e_Celular_/_Instituto_de_Investigac_¸ão_e_Inovac_¸ão_em_Saúde,_University_of_Porto, Portugal

j_Pulmonology_Department,_Vila_Nova_de_Gaia-Espinho_Hospital_Center,_Vila_Nova_de_Gaia,_Portugal k_Pulmonology_Department,_Instituto_Português_de_Oncologia_(IPO),_Coimbra,_Portugal

l_Pulmonology_Department,_Hospital_Pulido_Valente,_Centro_Hospitalar_Lisboa_Norte,_Lisboa,_Portugal m_Pulmonology_Department,_CUF_Infante_Santo_Hospital_and_CUF_Descobertas_Hospital,_Lisbon,_Portugal

n_{Comprehensive}_Health_Research_Centre,_Chronic_Diseases_Research_Center_(CEDOC),_NOVA_Medical_School,_Lisbon,_Portugal

Received24June2020;accepted16July2020

KEYWORDS Interventional pulmonology; Bronchoscopy; Thoracocentesis; COVID-19; Consensusstatement

Abstract Coronavirusdisease2019(COVID-19)isanemerginginfectiousdiseasecausedbya novelSARS-CoV-2pathogen.Itscapacityforhuman-to-humantransmissionthroughrespiratory droplets,coupledwithahigh-levelofpopulationmobility,hasresultedinarapiddissemination worldwide. Healthcare workershavebeenparticularly exposed tothe riskofinfection and representasigniﬁcantproportionofCOVID-19casesintheworstaffectedregionsofEurope.

Like otheropenairwayproceduresor aerosol-generatingprocedures,bronchoscopy poses a signiﬁcantrisk ofspreading contaminateddroplets, andmedical workersmustadaptthe

∗_{Corresponding}_author.

E-mailaddress:fernando.t.guedes@gmail.com(F.Guedes). https://doi.org/10.1016/j.pulmoe.2020.07.007

3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34

(2)

procedurestoensuresafetyofbothpatients andstaff.Severalrecommendationdocuments werepublishedatthebeginningofthepandemic,butasthesituationevolves,ourthoughts shouldnotonlyfocusonthepresent,butshouldalsoreflectonhowwearegoingtodealwiththe presenceofthevirusinthecommunityuntilthereisavaccineorspecifictreatmentavailable. Itis inthissense thatthis documentaimsto guideinterventional pulmonologythroughout thisperiod,providingasetofrecommendationsonhowtoperformbronchoscopyorpleural proceduressafelyandefficiently.

Introduction

Coronavirus Disease 2019 (COVID-19), a new infectious

disease that emerged in early December 2019 in Wuhan

Q6

(China),1_is_triggered_by_a_novel_pathogen_with_phylogenetic

similaritytowhatcausedthesevereacuterespiratory

syn-drome(SARS)outbreakin2003,andwascalledSARS-CoV-2.2

Itscapacityforhuman-to-humantransmissionand

interna-tionalair travelfacilitated the rapid disseminationon an

unprecedentedscaletotherestoftheworld.3,4

InItaly,thelatestﬁguresreportedthat9%ofCOVID-19

caseswerehealthcare workers(HCW),while inSpainthe

rateofmedicalstaffinfected reached26%, thehighestin

Europe.5_In_Portugal,_by_12th_May_2020,_11.3%_of_infections

occurredinHCW.6_There_are_at_least_two_explanations_for

suchahighnumberofinfectedpersonnel.First,thelackof

properpersonal protectiveequipment (PPE)at the

begin-ning of the epidemic, when assisting both conﬁrmed and

suspectedpatientswithCOVID-19.Second,thedurationof

exposuretoinfectedpatientsundergoingaerosol-generating

procedures,suchasnon-invasiveventilation(NIV)and

bron-choscopy,directlyresultinginasigniﬁcant increaseinthe

riskoftransmissiontoHCW.

The Portuguese Society ofPulmonology recentlyissued

aset of recommendations for bronchoscopicprocedures,7

shortly after the diagnosis of the ﬁrst cases in Portugal.

The documentaimedtoguaranteethe protectionof both

patientsandmedicalpracticioners,andtoensurethatthe

healthcare workforce would be conserved to fullﬁll their

mission throughout the period. Since then, a signiﬁcant

amount of scientiﬁc evidence has been accumulated; so,

thepresentdocumentgivesanupdateoftheavailable

lit-erature,providingpracticalsuggestionsfor pulmonologists

undergoingbronchoscopyorpleural proceduresinthe

set-tingofthecurrentandpost-pandemicphases.

Risk

of

transmission

Respiratory droplets comprise the main route of

SARS-CoV-2transmission, although airbornetransmission is also

possible through aerosol-generating procedures, such as

bronchoscopy.8 _One_study _during _the_H1N1 _pandemic

pro-videdexperimentalevidencethatbronchoscopicprocedures

increasesmorethan4timestheviralcopynumberperlitre

in positiveair samples.9 _While _the _heavy_droplets _rapidly

settle,aerosolparticles aremuchsmaller(<5−10␮m)and

aredispersedintheairover extensivedistances,posinga

considerablerisk ofinfectioninenclosedspaces,specially

ifpoorlyventilated.10

Thecontributionofasymptomaticcarriershasalsobeen

subject of debate.11,12 _A _signiﬁcant _proportion _of _them

have lung abnormalities onchest CT scans13,14 _and _a _high

levelofviralsheddingmaybedetectedinpresymptomatic

patients,14_so_it_is_likely_that_transmission_occurs_in_the_early

stagesofinfectionwhenpatientsareeitherminimally

symp-tomaticorasymptomatic.Unrecognizedpatientsposeareal

challengetoinfectioncontroland,whennotpromptly

han-dledwithappropriateairborneprecautions,areoneofthe

mostcriticalfactorsforSARS-CoV-2infectionspreadinthe

healthcaresetting.

Methods

ThePortuguesePulmonologySocietyappointedFGtochair

this consensus group. Seven national IP specialists were

selected based on their clinical expertise and different

settings (university vs. non-university hospitals; state vs.

private hospitals; pulmonologists vs.critical care

special-ists; ...).At theﬁrst online consensusmeeting, attended

byallmembers,aprimarydraftwithseveralsectionswas

created. This was sharedonline andfurther improved by

writtencommentsandsuggestions.Then,eachIPspecialist

wasassignedaspeciﬁcsectionpresentedinthisdocument

and wasresponsiblefor reviewing and evaluatingthe

rel-evant available literaturerelated tothe topic. Electronic

databases(Pubmed,OVIDMedlineandEmbase,Webof

Sci-ence,CochraneCentralRegisterofControlledTrials)were

usedtosearchfortheterms‘‘COVID-19’’OR‘‘SARS-CoV-2’’

AND(‘‘bronchoscopy’’OR ‘‘interventionalpulmology’’OR

‘‘thoracentesis’’OR ‘‘thoracocentesis’’OR‘‘pleural

effu-sion’’ OR ‘‘pneumothorax’’ OR ‘‘rigid bronchoscopy’’ OR

‘‘thoracoscopy’’ OR ‘‘chestdrain’’). Positionpapers from

major health organizations (US Centers for Disease

Con-trolandPrevention,EuropeanCentreforDiseasePrevention

andControlandWorldHealthOrganization)andimportant

scientiﬁcsocieties(EuropeanRespiratorySociety,European

AssociationforBronchologyandInterventionalPulmonology,

American Association for Bronchology and Interventional

Pulmonology,WorldAssociationfor Bronchologyand

Inter-ventional Pulmonology and British Thoracic Society) were

alsoreviewed. 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130

(3)

In a second online conference the complete draft was

evalutedbyallteammembersandtwoworkinggroupswere

created. They were responsible for discussing and

revis-ingdifferentsections,andeditingthetextforconsistency.

Afterwards, the ﬁnal manuscript was distributed to the

consensusgroupmembersandassessedforﬁnalapproval.

Adaptations

of

the

interventional

pulmonology

(IP)

department

Althoughthereisstillsomeheterogeneityinthedeﬁnition

andscopeof of‘‘interventional pulmonology’’(IP),it has

becomethemostwidelyacceptedtermtodescribetheuse

oftechniquesforthediagnosisandtreatmentofagrowing

numberofthoracicdisorders.15

In the context of this document, the term IP is used

to encompass the concepts of bronchoscopy (diagnostic

or therapeutic), advanced bronchoscopy (ﬂexible or rigid

bronchoscopy and all its associated techniques),

pleu-roscopy (rigid or semi-ﬂexible) and other simpler pleural

techniques (such as thoracentesis, placement of thoracic

drainagesystemsandindwellingpleuralcatheters).Though

weacknowledgethiswiderdeﬁnitionofIPmaybe

contro-versial,itcoversalltechnicaldomainsthatmostPortuguese

pulmonologistsneedtoaddress,andforthepurposeofthis

document,itpositionsustoissuegeneralrecommendations.

In the following subsections, speciﬁc scenarios of

differ-enttechnicalspecializationswillbeaddressed inorderto

overcomethisbroaderdeﬁnitionandtoapplyitbetterto

individualsettings.

The IP department is a high-risk area, given the type

ofproceduresthatareperformedwithairwaymanipulation

andwithmultiplestaffinvolved.Althoughthissettingis

gen-erallydesignedtodealwithoccasional airborneinfectious

diseases,suchastuberculosis,itisnotpreparedto

systemat-icallyassesshigh-riskcasesthatneedadditionalresources,

diminishproductivityandeffectivenessandgenerateahuge

workload.

Thus, each IP unit must rethink their administrative

andlogisticcircuitsindifferentareas,aswellasthetype

andtimingofperformedprocedures,toprotectbothHCW

and patients. Moreover, as international health

associa-tionsadvocate,aninfection-controlprograminhealthcare

settings should be implemented, consisting of a

three-levelhierarchy,includingadministrative,environmentaland

engineering controls, and personal protection equipment

(PPE).16 _In _the _following _subsections, _each _of _the _above

listedhierachiclevelsarebrieﬂypresented.

Administrativeandorganizationalissues

Administrativeand logisticmeasures are crucialto

ensur-ingsafetywhilestillmaintainingIPactivity.17_Some_general

precautionsinclude:

- Allreferralsandrequests totheIP unitmustpreferably

bemadebytelephoneordigitalmeans.

- Uponscheduleand24−48hpriortoarrivalattheIPUnit,

patientsshouldbecontactedbytelephoneandsubmitted

toapre-screeningchecklistthatincludesquestionsabout

1) recent symptomssuggestive of COVID-19 (e.g. fever,

cough,chills,musclepain,shortnessofbreath/difﬁculty

breathing,headache,sorethroat,lossoftasteorsmell);

2) contact withsuspicious/conﬁrmed SARS-CoV-2cases;

and3)occupationalexposure.

- Patientswhohaverecentrespiratoryandinfectious

symp-tomsand/orchestimagingsuggestiveofCOVID-19,should

havetheirelectiveprocedurespostponedandrescheduled

afterallsymptomsareresolved.

- On arrival at the IP Unit, all patients must be asked

again for respiratory symptoms and have their

temper-aturechecked.

- Ifpossible,allpatientsshouldhaveatleastonenegative

RT-PCRforSARS-CoV-2inthe24−48hprecedingtheexam.

InpatientswithapositiveRT-PCRSARS-CoV-2,the

deci-siontoprocedewiththeinterventionwillbebasedonthe

urgencyoftheprocedure(Chart1andTable1).

- The IPunitshouldkeeparecordofdeferred patientsto

reschedule their procedures according to the COVID-19

outbreaksituation,asproposedinTable2.

Environmentalandengineeringcontrol

Physicalspacepreparation

The design of strategies to minimizerisks and a protocol

ﬁttingthecharacteristicsofeachspeciﬁcUnitarecrucial.18

- Reception, administrative, clinical and waiting areas

should separate conﬁrmed/high-risk patients from

negative/low-riskones.Inaddition,inpatientsshouldbe

segregated fromoutpatients,either by timeor physical

location,topreventcrossinfection.

- Speciﬁc circuits and written workﬂow plans must be

prepared, coveringthe pre-procedural area,procedural

room,post-proceduralarea,decontaminationand

repro-cessing.Theimplementationofaﬂowchartwithdifferent

areas and walking pathsusing a visual colour zone

sys-temcan beuseful:1)red zonefor contaminatedareas;

2)yellowzonefortransitionareas,and3)greenzonefor

non-COVID-19safeareas19₍_Fig.₁_A)._These_need_to_be

for-mulatedby internal elements fromtheIP unitwiththe

cooperationofamultidisciplinaryteamofhospital

mem-bers, includingadministration, engineers,and infection

controlboard.

- Aspeciﬁc placetostoreand retrieveallitems required

forPPEshouldbedeﬁnedinsidetheUnit.

- AdesignatedareaintheUnitshouldbeselected,closeto

theproceduralsuite,forgowningandremovalofallPPE,

accordingtohospitalprotocolandstandards,inorderto

reduceexposuretocontaminatedparticlesanddroplets.

Whenananteroomisavailable,itmaybeusedasanarea

fordonninganddofﬁngofPPE(Fig.1B).

- Stations should be created to facilitate frequent hand

hygieneandtodistributewaste containersaccording to

local infectious control recommendations. Posters and

other visualaids shouldbeplacedat strategiclocations

aroundtheinterventionsuitetoactasreminders.

- Emergency procedures in COVID-19 positive patients

should preferably be performed within the ICU

enviro-ment,withcontrolledairwaythroughcuffedendotracheal

tubeandassistedventilation.

131 132 133 134 135 136 137 138 139 140 141 142 143 144 145 146 147 148 149 150 151 152 153 154 155 156 157 158 159 160 161 162 163 164 165 166 167 168 169 170 171 172 173 174 175 176 177 178 179 180 181 182 183 184 185 186 187 188 189 190 191 192 193 194 195 196 197 198 199 200 201 202 203 204 205 206 207 208 209 210 211 212 213 214 215 216 217 218 219 220 221 222 223 224 225 226 227 228 229 230 231 232 233 234 235 236 237 238 239 240 241 242 243

(4)

Chart1 ProposedtriageofIPproceduresQ1 duringtheCOVID-19outbreak.

(5)

Table2 ScheduleofIPproceduresaccordingtothestage ofCOVID-19pandemic.

COVID-19inthecommunity IPUnit Exponentialincreaseofnew

cases

Urgentcases---only Rapidincreaseofnewcases Urgentcases--- only

Electivebutnotdelayable ---evaluatecase-by-case Decreaseinnewcases Urgentcases---fullcapacity

Elective,butnotdelayable ---fullcapacity

Electiveanddelayable ---resumepartialcapacity Absenceofnewcasesinthe

last2weeks

Resumeallcaseswithfull capacity

- ElectiveproceduresshouldbereservedforCOVID-19

neg-ativepatients(Chart1andTable1).Nevertheless,these

proceduresshouldstillbeperformedinadedicated

neg-ativepressureroom(seebelow,ventilationrequirement)

withstrictisolationprecautionsandsufﬁcientventilation

toavoid aerosol contamination.20 _If _these_requirements

arenotmetinthebronchoscopysuite,theninadifferent

venue,suchasanoperatingtheatre,isolationroomorthe

ICUwithnegativepressure,ifavailable.

- Ifnegativepressureroomsareunavailablethrougoutthe

instituition,aspeciﬁcanddedicatedroomwithadequate

natural ventilation (see requirement below) may be an

alternative,providedthatappropriateintervalsbetween

proceduresarereservedandthatthesuspectedCOVID-19

casesbeprogrammed afterallplannednon-COVID daily

activity,sothattheunitcanbecarefullycleaned

(follow-ingthedisinfectionpolicy)andventilated.

- Keeptheendoscopyroomfor proceduresonly(allother

activities,suchasplanning,reportingandlaboratory

req-uisitionshouldtakeplaceelsewhere).

- Suspected and conﬁrmed cases of COVID-19 must be

placedinan airborneinfectionisolation roomwith

neg-ativepressurebeforeandafter theprocedure.Low-risk

andnegativepatients can remainin the pre-procedural

andrecoveryarea,ifthereisadequateroomventilation,

protective equipment (e.g. surgical mask) and physical

distance(>2m)fromothernegativepatients.

Ventilation

- Patientsourcecontrolstrategies,suchaswearingamask

shouldbeencouraged.

- Whenever feasible, it is recommended procedures are

pereformedinaroomthatmeetstheventilation

require-mentsforAirborneInfectionIsolation(AII), ensuringthe

dilutionandremovalofcontaminatedair.The preferred

system is a negativepressure roomwithat least 12 air

changes per hour (ACH) with airﬂow direction control

(single-passorrecirculationsystemswithHEPAﬁltration).

Alternatively, natural ventilation with an airﬂow of at

least160L/sisanoption.19,21

- Enough time should beallowed to ensure that

contam-inated air is removedfrom theroombefore performing

anotherprocedureinthesameroom(dependingonACH

and disinfection methods, but at least 30min). Local

adaptationsmustbeconsideredaccordingtothe

charac-teristicsoftheIPunit.

Cleaninganddisinfectingpatientcareequipmentand rooms

Endoscopes are considered semi-critical medical

instru-ments according to the Spaulding classiﬁcation.22

Rec-ommendations from the Centers for Disease Control

and Prevention (CDC) on reprocessing procedures should

be followed. These include pre-cleaning, leak-testing,

manualcleaningandvisualinspectionfollowedby

disinfec-tion/sterilization.

- A high-level manual disinfection or using an automated

endoscopereprocessorisrecommended.

- Proper storage and documentation are also an integral

partofthereprocessingworkﬂow.

- Apathwayofcontaminatedequipmentmustbedeﬁned,

aswellasadequatepackagingtominimizeexposure(for

example,ahermeticbox).

- Ifavailable,disposablebronchoscopesarerecommended

forconﬁrmedCOVID-19patientswithclearadvantagesin

portability,post-procedural handling andcross

contami-nationrisk.23

Figure1 A.Implementationofspeciﬁccircuitswithcolourvisualzonesystemtodistinguishcontaminated(1,redzone),transition (2,yellowzone)andsafecleanedareas(3,greenzone).B.DesignatedareafordonninganddofﬁngofPPE,wherepostersandother visualaidswereplacedstrategicallytoactasreminders.

244 245 246 247 248 249 250 251 252 253 254 255 256 257 258 259 260 261 262 263 264 265 266 267 268 269 270 271 272 273 274 275 276 277 278 279 280 281 282 283 284 285 286 287 288 289 290 291 292 293 294 295 296 297 298 299 300 301 302 303 304 305 306 307 308

(6)

Table3 SpeciﬁcationsforpersonalprotectiveequipmentduringIPprocedures. PPE Characteristics/speciﬁcations/standards Observations Gloves Single-use

Waterproof

StandardENISO374-2:2014, 374-3:2014e374.5:2016 Doublegloves:

-ﬁrst:longsleevedgloves -second:nitrilegloves EyeProtection Goggleswithlateral

protection

Ifnotforsingleuse,performdisinfectionwith ethanolbasesolutionor0.1%sodiumhipochlorite Faceshield

Gowns Single-use ConsiderbiologicalriskprotectionEN14126:2004, ifconﬁrmedpositivepatient

Waterproof Longsleeved

StandardEN14605:2009

Cap Single-use Considerhoodcap,ifconﬁrmedpositivepatient Shoecover Single-use

Respiratory FFP2/N95 Performsealcheckbeforeentertheendoscopy suite.

Protection Single-use ConsiderFFP3,ifconﬁrmedpositivepatient PPE,personalprotectiveequipment.

- Floorsandsurfacesoftheendoscopysuitemustbe

disin-fectedaftereachprocedure.

- Intermediate level disinfectants with proven activity

againstenvelopedviruses include0.1%sodium

hipochlo-rite, 62---71% ethanol, 0.5% hydrogen peroxide and

quaternaryammoniumcompounds.19,24,25

Personalprotectiveequipment

IPproceduresareconsidered tobeconsistentlysubjected

tothehighestriskofexposure.Inthissetting,full

precau-tions must be taken to cover all different possible types

of transmission(contact, dropletand airborne).26

Person-nelinvolvedinthereprocessing proceduremustalsowear

protectiveequipmentconsistingofeyeprotection,

respira-torymaskFP2,longsleevedgownanddoublegloves.27,28_The

recommendationsfortheuseofPPEareshowninTable3.

Specimentransportation

Samplesfromtheupperandlowerrespiratorytract,

includ-ingpleuraleffusion,aredeemedtobethemostpotentially

infectious.Consequently,theyshouldbe handledas

Cate-gory3pathogenanddouble-bagged(ﬁrstthespecimenmust

bebaggedinthepatient’sroomandthentakenoutofthe

roomandplacedinaseparatepre-labeledspecimenbag).

Allspecimensmustbemanuallydelivered.28,29

Safety

rules

for

staff

and

patients

ItisalsoimportanttodeﬁnepropernewrulesforbothHCW

andpatientscirculatingintheIPunit,aslistedbelow:

Healthprofessionals

- TheIPUnitshouldreduceandprioritisetheallocationof

humanresourcesaccordingtotheoutbreakevolutionand

hospitalneeds.Theminimumnumberofstaffrequiredto

ensureacorrectoperationmustbeclearlydeﬁned.

- Itisessentialthatallpersonnelfollow,trainandmaintain

competencyineffectivehandhygieneandeveryaspectof

PPE(theoretical,trainingandsimulationsessions)sothat

everyoneisfamiliarwiththeirrole.

- All interactions with patients, including informed

con-sent,shouldbedone withappropriatePPEandfrequent

hand washing.The staffshould not reduce the level of

awarenessandprotection,andtheideathatpatientswith

suspectedCOVID-19shouldbehandledinthesamemanner

asconﬁrmedcasesmustbereinforced.

- A core team that includes only essential HCW should

performtheprocedure onSARS-CoV-2positive patients.

Themostexperiencedstaffshouldberesponsibleforthe

exam toreduce timeand dealeffectivelywith possible

complications.Otherhealthcarepersonnel,suchas

resi-dents,medicalstudentsandvisitorsshouldnotbeinside

theunitandtheexaminationroombefore,duringorafter

theprocedure.

- Ofnote,thescheduledexamsmustbedoneduringnormal

working hours (avoiding an emergency basis or setting)

andinanappropriate,designatedroomthatfulﬁlsallthe

standardsrequiredforcare.

Patientsandotherpersonel

- Respiratoryandcontactisolationshouldbestandardand

mandatory for all patients. Outpatients and inpatients

shouldalwaysentertheIPUnitwithasuitablefacemask

309 310 311 312 313 314 315 316 317 318 319 320 321 322 323 324 325 326 327 328 329 330 331 332 333 334 335 336 337 338 339 340 341 342 343 344 345 346 347 348 349 350 351 352 353 354 355 356 357 358 359 360 361 362 363 364 365

(7)

andkeepitonatalltimes(untilthebeginningandafter

theendoftheprocedure)tominimizetheriskof

trans-mission.Nounnecessarypersonalitemsshouldbebrought

intotheIPunit.

- Familymembersandcaregivers shouldnotstayintheIP

waitingrooms.Incaseofchildrenorpatientsinneedof

support,theUnitcanallowasinglerelativetoenterthe

preparationareatoprovideaid.

- TheentryintotheUnitofsuppliersandmedicaldevices

salesrepresentativesmustberestricted.

Prioritization

of

procedures

Scheduledelectiveproceduresshouldbereviewedand

can-celled if potentially delayable, until local control of the

outbreakisachieved.Afterﬂatteningtheinfectiouscurve,

manyelectiveIPprocedureswillhavetobeperformed,as

theyareessentialtoprovideadeﬁnitivediagnosisand

effec-tivetreatment.Atthistime,itisadvisabletoevaluatethe

delayed requests and tooptimizethe procedure planning

basedonclinicalneedsandoperationalcapability.

A suggestedrational approachfor stratiﬁcation of

pro-cedures is providedin Table 1, but we recognize that,in

certain cases,the indication may notbe straightforward,

andtherisk-beneﬁtmustbeweightedonanindividualbasis

bytheIPteam.31 _Although_rescheduling_certain_procedures

is obvious in other cases it may not be desirable or

eth-ical. It is important to note that these indications may

change according to local epidemiological conditions and

theresponsecapabilitiesofthehealthcaresystem.Several

societieshave recommendeddifferentlevelsofprocedure

stratiﬁcation.26,30,31_Brieﬂy,_what_is_recommended_is_a

step-wisereopeningof electiveIP proceduresaccording tothe

nationalandlocalCOVID-19outbreaksituation,depending

onthenumberofnewconﬁrmed cases,hospitaladmitted

cases(wardandICU),availabilityofequipmentand

health-carestaff,timeelapseandnumberofpostponedIPcases.

Some authors34 _have _proposed _a _summary_of _the _elective

endoscopicprocedurebyphases,asshowninTable2.

Any-way,itshouldbenotedthattheevolvingproceduralcriteria

should always be communicated to other physicians who

referpatientsforinvasiverespiratoryproceduresandtothe

hospitaladministration.

Recommendations

for

bronchoscopy

Bronchoscopyunderspontaneousventilation

The following reccomendations are expert opinion-based

andshouldbeadaptedtolocalregulationsandguidelines.

In an optimal scenario, it is safer to perform elective

bronchoscopy under general anesthesia and orotracheal

intubation,clinicalconditionspermitting.Ifthisisnot

pos-sible, bronchoscopy canbe performed under spontaneous

ventilation.Somerecommendationsarelistedbelow:

- Operatorshouldbestandingbehindthepatient’sheadto

reducedirectexposure. Oxygensupplementationshould

bedonewithouttheuseofhumidiﬁcation,eitherthrough

anasalcannulaor preferablywithan oxygenmask with

anentrancetothebronchoscope(Fig.2A).

- Forﬂexiblebronchoscopy,atransnasalapproachshouldbe

preferred,andasurgicalmaskshouldbeplacedoverthe

patient’smouthtominimizedropletemission(Fig.2B).

- In hypoxemic patients, bronchoscopy can be performed

underNIV, usinga closedcircuitventilation (double

cir-cuit with viral ﬁlters in both arms) and non-ventilated

maskswithadedicatedbronchoscopeentrance(Fig.2C).

HighperformanceNIVventilatorswithFiO2regulationare

preferable.Fromtheendoftheprocedure,NIVshouldbe

continuedfor1−2h,titratingtheFiO2toobtainanSpO2

ofaround94---95%.

- Bronchoscopyundernasalhigh-ﬂowoxygentherapyisnot

reccomendedandthusshouldbeavoided.

- Nebulizedmedicationsshouldbeavoidedbeforeorafter

theprocedure.

- Propersedationshouldbeusedtominimizecoughreﬂex

andtoincreasepatientcooperation.

- Anoralaspirationcannulashouldbeavailableduringthe

procedure(Fig.2B).

- Atransparentprotectiveboxmayenhancesafetyby

con-tainingdispersalofdropletparticles(Fig.2D).Theboxis

placedoverthepatient’sheadpriortobronchoscopy,with

theanesthesiaequipmentalreadyinplace.The

broncho-scopeisinsertedthroughthecoveredopeningbehindthe

patient(Fig.2E).

Bronchoscopyintheintubatedpatient

The following recommendations are directedfor patients

under mechanical ventilation in an ICU setting due to

respiratory failure. As reported, 5% of COVID-19 patients

can develop respiratory failure and will need ventilatory

support32_; _moreover, _associated _bacterial, _viral _and

fun-gal co-infection should not be negleted.33 _In _critically _ill

patients under invasive ventilation, ventilator-associated

pneumonia occursin up to30% andlobar collapse is

fre-quentandmultifactorial.34 _The _same_adaptations_apply_to

electiveproceduresundergeneralanesthesia,performedin

theBronchoscopyUnitorOperatingTheatre.

- Acuffedendotrachealtubeispreferredoversupraglotic

devices,suchasalaryngealmask;cuffpressureshouldbe

maintainedbetween25---30cmH2O.35

- Generalanesthesiawithmusclerelaxantisrecommended

toreducetheaerosolproduction.

- FiO2shouldbeadjustedto100%.

- Volumecontrol,pressure-limitedmodeispreferableand

PEEPshouldbekeptatthesamelevelduringthe

proce-dure.Adjustmentscanbemadedynamically,withaprior

assessmentoftheanticipatedrisks(e.g.,lung

derecruit-mentanddesaturation,arrhythmias,pneumothorax).

- To avoid aerosol dispersion, a simple and appropriate

maneuverconsistsofclampingtheventilationcircuitjust

beforeintroductionofbronchoscope,repeatingthesame

stepjustbeforewithdrawal.

- Bronchoscoperemovalandreinsertionshouldbeavoided

duringtheprocedure.

- Inhypoxemicpatients,ifbronchoalveolarlavageisneeded

for diagnostic purposes, the volume used should be

366 367 368 369 370 371 372 373 374 375 376 377 378 379 380 381 382 383 384 385 386 387 388 389 390 391 392 393 394 395 396 397 398 399 400 401 402 403 404 405 406 407 408 409 410 411 412 413 414 415 416 417 418 419 420 421 422 423 424 425 426 427 428 429 430 431 432 433 434 435 436 437 438 439 440 441 442 443 444 445 446 447 448 449 450 451 452 453 454 455 456 457 458 459 460 461 462 463 464 465 466 467 468 469 470 471 472 473 474 475 476

(8)

Figure2 Strategiestominimizedropletsdispersal duringbronchoscopy.A.The bronchoscopemay beintroducedthroughan openingmadeattheoxygenmask,inthiscasewithanadditionalplasticsheetcoveringthepatient’shead.B.Transnasalapproach, withoxygensupplementationthroughnasalcannulaandasurgicalmaskplacedoverthepatient’smouthandtheoralaspiration canulla.C.Bronchoscopycanbeperformedunderventilatorysupport,usingaclosedcircuitventilationandnon-ventilatedmasks withadedicatedbronchoscopeentrance.D.Transparent protectivebox maycontaindropletparticlesinside.E.Protective box placedoverthepatient’sheadduringendobronchialultrasound.F.Rigidbronchoscopywithrubbercapsontheportsofthescope andaplasticcovering.

reduced to a minimum. If a SARS-Cov-2 diagnosis is

needed, a minimum of 2−3mL of recovered lavage is

enough.26

Rigidbronchoscopy

Rigid bronchoscopy is used for diagnostic and

therapeu-tic purposes, in procedures where ﬂexible bronchoscopy

wouldbedeemeddifﬁcultorevenimpossible,like

obtain-ing largersamples of endobronchial lesions, foreignbody

removal,managementofcentralairwayobstruction

(includ-ingablativetechniques, likeelectrocautery,argonplasma

coagulation,laser, cryotherapy, among others,and

place-mentofairwaystents)ormassivehemoptysis.36

There are different ventilation strategies used during

rigidbronchoscopy,althoughmanualjetventilationandhigh

frequency jet ventilation are much the most frequent.37

Commontothesetwotechniquesisthefactthatthe

prox-imalendofthebronchoscopeisopentoallowthepassage

ofinstruments,thusventilationisachievedproviding100%

oxygenunderhighpressure(usually50psi)throughanopen

system.39,40 _The_use_of_these_ventilation_techniques_means

thataerosolsarereleasedintotheroom,makingita

high-riskprocedure.

Inpatientswithsuspectedor conﬁrmedCOVID-19

diag-nosis, rigid bronchoscopy should be avoided, except for

urgent cases (Table 1). Clinical scenarios are mostly

therapeutic, like acute foreign body aspiration, massive

hemoptysis (when there is no place for embolization),

severe symptomatic central airway obstruction (either

benign or malignant) and migrated stents. In a clinically

stable patient,upon suspicion of foreignbody aspiration,

oneshouldconsidernon-contrastcomputerizedtomography

(CT)toconﬁrmthepresenceofaforeignbodybeforerigid

bronchoscopy,toavoidunnecessaryexams.38,39

Insomecenters,therigidscopeisusedtoperformother

techniques, like Endobronchial Ultrasound-Transbronchial

Needle Aspiration (EBUS-TBNA) or transbronchial

cry-477 478 479 480 481 482 483 484 485 486 487 488 489 490 491 492 493 494 495 496 497 498 499 500 501 502 503 504 505 506 507 508 509 510 511 512

(9)

obiopsy;thisprovidescomforttotheoperatorandsafetyin

case ofmajorbleeding.The authorsrecommend

perform-ingthesediagnosticproceduresthroughcuffedendotracheal

tubetominimizetheriskofexposure.However,theoperator

mustbereadytoconverttorigidbronchoscopy,ifnecessary.

Inapatientundergoingrigidbronchoscopy,itis

recom-mendedthat:

- Rigidbronchoscopyshouldalwaysbeperformedina

neg-ativepressureroom.

- Controlled ventilationis preferred, withthe rigid

bron-choscopeusedlikeanendotrachealtube.

- Air leaks should be reduced using rubber caps on the

portsoftherigidscope,aswellasusingaplastic

cover-ing(Fig.2F)orﬁllingthemouthwithgauze.40_While_this

strategy is more appealing tominimize aerosol spread,

theoperatormayﬁnditchallengingtohandleinstruments

throughtheworkingchannel.

Recommendations

for

pleural

techniques

Pleuraleffusiondoesnotappeartobeaprominentfeature

ofCOVID-19.Itoccursin5.3---5.8%ofpatients,accordingto

tworecentmeta-analyses.41,42_There_have_been_occasional

reportsofbilateraleffusion thatresolvedspontaneously.43

As bacterial superinfectionis common in severe patients,

theycanalsodevelopcomplicated effusionsor empyema,

requiring targeted treatment. There have been a few

anecdotalreportsofspontaneouspneumothoraxand

pneu-momediastinum in severe COVID-19 pneumonia, requiring

drainage.44,45_This_may_be_more_frequent_in_critical_patients

oninvasive ventilation, which can leadto bronchopleural

ﬁstulae.46 _It _is, _therefore, _plausible _that_pleural _drainage

maybenecessaryinsomeCOVID-19patients,eitherinthe

ICU or in the ward, and indications for drainage do not

differ from the standard clinical guidelines. However, as

withanyinvasiveprocedureinconﬁrmedCOVID-19patients,

allprecautions regardingthe fulluse ofprotective

equip-ment shouldbetaken.The procedure must beperformed

by trainedanddedicated stafftoreduce itsduration and

tominimizetherisk of complications.In othersituations,

the use of ultrasound may be very helpful with

COVID-19patients.47 _Besides _its_wide_{availability,}_safety_and_low

cost, it is easy to use at the bedside andallows medical

stafftodetect smallpleuraleffusionsandtoguidepleural

ﬂuidcollectionanddrainage,ifneeded.Ontheotherhand,

evenpatientswithoutsuspectedCOVID-19canhave

assymp-tomaticinfection;so,anyprocedureshouldbeconsideredas

apossibleCOVID-19caseandprecautionsshouldbetaken.

Indeed, although some procedures may be postponed, in

manysituationstheyshouldnotbedeferred, especiallyin

suspected or conﬁrmed cancer patients. It is crucial that

cancer patients donot experiencedelays in diagnosticor

therapeuticproceduresduetothepresentcontingency.48

Fewsocietieshavepublishedguidelinesaddressing

pleu-ral procedures during COVID-19 pandemic. The British

Thoracic Society has issued guidance on pleural

ser-vices provision,49 _mainly _to _minimize _hospital _visits _and

admissions and to ensure both patient and staff safety.

Nonetheless,althoughwe recognizelack ofpublished

evi-dence supporting these reccomendations, this document

willadoptsomeofthem.

Firstofall, despitepleural proceduresnotbeinglisted

asAerosolGeneratingProcedure(AGP)intheCDCupdated

reccomendations,50_they_should_be_considered_so_and_Level

2PPEshouldbeworn,asdescribedabove.Othersocieties

have considered potential AGP as any procedure ‘‘likely

toinduce coughing, that should beperformed cautiously andavoided ifpossible’’.51 _This_is _particularly_relevant _to

openprocedures,suchasthoracoscopyandindwelling

pleu-ral catheterinsertion, and in case of pneumothorax with

suspected bronchial-pleural ﬁstula. Thus, we recommend

takingthefollowingprecautions:

Pleuraleffusion

- Onsuspicionofmalignanteffusion,diagnosticpleuralﬂuid

aspirationshouldbeperformed,especiallyifthepatient

is a candidatefor systemictherapy or ifthe effusion is

symptomatic(Table1).

- Consider placement of indwelling pleural catheters for

recurrentmalignantpleuraleffusions,avoidingrepeated

hospitaldrainageoradmission.

- Onsuspicionofpleuralinfection,pleuralﬂuidaspiration

andanalysisshouldbeperformed.

- Incaseofbenignpleuraleffusions,therisk-beneﬁtshould

bediscussedwiththeattendingphysician;procedurescan

bepostponedifthepatientisnotsymptomatic.

- Thoracoscopy is not recommended as a principle;

how-ever,intheabsenceofalternativeoptions,itsrisk-beneﬁt

mustbeassessed.

Pneumothorax

- Spontaneous primarypneumothorax can be managed in

outpatientcareiftheriskassessmentallowsandifthere

islocalteamexperience;needleaspirationanddischarge

should be considered if the patient is minimally

symp-tomatic.

- Whenpleuraldrainageplacementisnecessary,ifthereis

localexpertiseandthepatientisat lowrisk,theuseof

pleuralventsystemsshouldbeconsidered,thusallowing

thepatienttobemanagedathome.

Chestdrainageplacementandcare

- Extracaremustbetakenwhenplacingthechesttubes,in

ordertoavoidopencommunicationwiththepleuralspace

andthepotentialemissionofdropletsandaerossols.

- Whenchesttubesareplacedinventilatedpatients,

con-sideration should be given to clamping the ventilator

circuitbeforeassessingthepleuralcavity,sothatpositive

pressurespreadingofpleuralairorﬂuidcanbeprevented.

- Wheneverpossible,theuseofnon-wiredpleuraldrainage

shouldbeconsidered;itcanbeconnectedtothedrainage

systembeforeinsertionintothepleuralcavity(closed

cir-cuit).

- When pleuroscopyisrequired,theuse ofonewayvalve

trocars should bepreferredto assessthe pleural cavity

andproperlysealtheentranceportofthepleuroscope.

513 514 515 516 517 518 519 520 521 522 523 524 525 526 527 528 529 530 531 532 533 534 535 536 537 538 539 540 541 542 543 544 545 546 547 548 549 550 551 552 553 554 555 556 557 558 559 560 561 562 563 564 565 566 567 568 569 570 571 572 573 574 575 576 577 578 579 580 581 582 583 584 585 586 587 588 589 590 591 592 593 594 595 596 597 598 599 600 601 602 603 604 605 606 607 608 609 610 611 612 613 614 615 616 617 618 619 620 621 622 623

(10)

Table4 IPUnitchecklistduringCOVID-19outbreak.

- In case of prolonged air-leaks, the use of wall suction

shouldbeweightedtocreateaclosedsystem.

Concluding

remarks

As with other societal consensus papers, this document

was developed by a restricted panel of experts from

the Portuguese Society of Pulmonology; individual

clini-caljudgmentand local resourcesmay lead toalternative

perspectives.Thisguidancewasbasedonthecurrent

knowl-edgeofCOVID-19,but,asnewdataappears,thisstatement

shouldbe revised in the futureto accommodate updated

recommendations. At present, one of the controversial

assumptionsis that,every patient,evenifasymptomatic,

shouldbeassumed aspotentially infected with

SARS-CoV-2.Therefore,itismandatorythatcontactprecautionsand

propertrainingondonninganddofﬁngof PPEbeprovided

toallHCWsinvolved inIP.Anotherkeyelementis toplan

inadvanceandkeepeachIPUnitwell-organized(Table4).

Althoughthereductioninthenumberofelectiveprocedures

representsoneofthecentralstrategiestoimprovesafety,

itiscrucialthatpatientsdonotsufferunnecessarydelaysin

diagnosticortherapeuticproceduresduetothecurrent

con-tingency.Takentogether,ourultimateintentionistobring

fullattentiontothisandfutureoutbreaksorotheremerging

medicalsituations.

Conﬂicts

of

interest

Theauthorshavenoconﬂictsofinteresttodeclare.

Q7 Q8

References

1.Huang C, Wang Y, Li X, Ren L, Zhao J, Hu Y, et al. Clinicalfeatures of patients infectedwith 2019 novel coro-navirus in Wuhan, China. Lancet. 2020;395(10223):497---506,

http://dx.doi.org/10.1016/S0140-6736(20)30183-5.

2.ZhuN,ZhangD,WangW,etal.Anovelcoronavirusfrompatients Q9 withpneumoniainChina,2019.NEnglJMed.2020;382:727---33.

3.Lu R, Zhao X, Li J, Niu P, Yang B, Wu H, et al. Genomic characterisationandepidemiologyof2019novelcoronavirus: implications for virus origins and receptor binding. Lancet. 2020;395(10224):565---74.

4.World Health Organization (WHO). Coronavirus disease 2019 (COVID-19)situationreport99;2020.

5.European Center for Disease Prevention and Control. Coro-navirus disease 2019 (COVID-19) in the EU/EEA and the UK---eighthupdate,8April2020. https://www.ecdc.europa. eu/sites/default/ﬁles/documents/covid-19-rapid-risk-assessment-coron avirus-disease-2019-eighth-update-8-april-2020.pdf (accessed on15thJune2020).

6.https://covid19.min-saude.pt/(accessed15thJune2020).

7.https://www.sppneumologia.pt/uploads/subcanais2conteudosﬁcheiros /posicao-da-spp-para-a-realizacao-de-broncoscopias-durante-a-pandem ia-do-coronavirus-(2).pdf(accessedon15th_June_2020).

8.Wilson NM, Norton A, Young FP, Collins DW.Airborne trans-mission of severe acute respiratory syndrome coronavirus-2 to healthcare workers: a narrative review. Anaesthesia. 2020;(April),http://dx.doi.org/10.1111/anae.15093.

9.Thompson KA, Pappachan JV, Bennett AM, et al. Inﬂuenza aerosolsinUKhospitalsduringtheH1N1(2009)pandemic----the riskofaerosolgenerationduringmedicalprocedures.PLoSOne. 2013.PMID:23418548.

10.TellierR,LiY,CowlingBJ,TangJW.Recognitionofaerosol trans-mission ofinfectious agents:a commentary. BMC Infect Dis. 2019;19,101-101. 624 625 626 627 628 629 630 631 632 633 634 635 636 637 638 639 640 641 642 643 644 645 646 647 648 649 650 651 652 653 654 655 656 657 658 659 660 661 662 663 664 665 666 667 668 669 670 671 672 673 674 675 676 677 678 679 680 681 682 683

(11)

11.MizumotoK,KagayaK,ZarebskiA,etal.Estimatingthe asymp-tomatic proportion of coronavirus disease 2019 (COVID-19) caseson boardthe DiamondPrincess cruiseship,Yokohama, Japan,2020.EuroSurveill.2020.PMID:32183930.

12.NishiuraH,KobayashiT,MiyamaetT,etal.Estimationofthe asymptomaticratioofnovelcoronavirusinfections(COVID-19). IntJInfectDis.2020.PMID:32179137f.

13.InuiS,FujikawaA,JitsuM,KunishimaN,etal.ChestCTﬁndings incasesfromthecruiseship‘‘DiamondPrincess’’with Coron-avirusDisease2019(COVID-19).Radiol:CardiothoracImaging. 2020;2(2):e200110.

14.ZouL,RuanF,HuangetM,etal.SARS-CoV-2ViralLoadinUpper RespiratorySpecimensofInfectedPatients.NEnglJMed.2020. PMID:32074444.

15.Seijo LM, Sterman DH. Interventional pulmonology. NEJM. 2001;344(10):740---9.

16.WHOTechnicalguidance.https://www.who.int/emergencies/diseases /novel-coronavirus-2019/technical-guidance/infection-prevention-and-control,2020(accessedon15thJune2020).

17.Centers for Disease Control and Prevention. Interim Infec-tion Prevention and Control Recommendations for Patients with Suspected or Conﬁrmed Coronavirus Disease 2019 (COVID-19) in Healthcare Settings. CDC. 13 April 2020.

https://www.cdc.gov/coronavirus/2019-ncov/hcp/infection-control-reco mmendations.html(accessedon15thJune2020).

18.BaldwinD.R.,LimW.S.,RintoulR.,NavaniN.,FullerL., Wool-houseI., etal.Recommendations fordaycasebronchoscopy servicesduringtheCOVID-19pandemic.BritishThoracic Soci-ety.Version1.2.March2020.

19.WorldHealthOrganization.HealthSystemsRespondto COVID-19TechnicalGuidance#2Creatingsurgecapacityforacuteand intensivecareRecommendationsfortheWHOEuropeanRegion 6April2020.

20.Adhikari U, Chabrelie A, Weir M, Boehnke K, McKenzie E, Ikner L, et al. A case study evaluating the risk of infec-tion from middle eastern respiratory syndrome coronavirus (MERS-CoV)inahospitalsettingthroughBioaerosols.RiskAnal. 2019;39(12):2608---24.

21.AmericanInstituteofArchitects.Guidelinesfordesignand cons-tructionofhospitalandhealthcarefacilities,2001.Washington, DC:AmericanInstituteofArchitectsPress;2001.

22.RutalaWA,Weber DJ. Disinfection ofendoscopes:review of newchemicalsterilantsusedforhigh-leveldisinfection.Infect ControlHospEpidemiol.1999;20:69---76.

23.WahidiMM,LambC,MurguS,etal.AmericanAssociationfor BronchologyandInterventionalPulmonology(AABIP)statement ontheuseofbronchoscopyandrespiratoryspecimencollection inpatients withsuspected or conﬁrmedCOVID-19infection. March9, 2020 and expert consensus ofthe AABIP COVID-19 Task Force. J Bronchology Interv Pulmonol. 2020;(March), http://dx.doi.org/10.1097/LBR.0000000000000681

https://aabronchology.org/wp-content/uploads/2020/03/2020-AABIP -Statement-on-Bronchoscopy-COVID.GAE-updated-Version.pdf (accessedon15thjune2020.

24.Centers for Disease Control and Prevention. Guideline for Disinfection and Sterilization in Healthcare Facil-ities, 2008. May 2019 update. https://www.cdc.gov/ infectioncontrol/pdf/guidelines/disinfection-guidelines-H.pdf (accessedon15thjune2020).

25.ChenCC,ChiCY. Biosafetyinthepreparationandprocessing of citology specimens with potential coronavirus (COVID-19) infection: perspective from Taiwan. Cancer Cytopathol. 2020;128(May(5)):309---16.

26.Tran K, Cimon K, Severn M, et al. Aerosol generating proceduresandriskoftransmissionofacuterespiratory infec-tionstohealthcare workers: a systematicreview. PLoSOne. 2012;7:e35797.

27.Healthcare Infection Control Practices Advisory Committee. Essential Elements of a Reprocessing Program for Flexi-ble Endoscopes --- The Recommendations of the Healthcare InfectionControlPracticesAdvisoryCommittee(HICPAC).2016. https://www.cdc.gov/hicpac/pdf/ﬂexible-endoscopereprocessing.pdf (accessedon15thJune2020).

28.PritchettMA,ObergCL,BelangerA.Societyforadvanced bron-choscopyconsensusstatementandguidelinesforbronchoscopy andairwaymanagementamidtheCOVID-19pandemic.JThorac Dis.2020;12(5):1781---98.

29.World Health Organization (WHO). Laboratory testing for Coronavirus Disease 2019 (COVID-19) in sus-pected human cases: interim Guidance, 19March 2020. https://www.who.int/publications/i/item/10665-331501 (accessedon15thJune2020).

30.Mazzone PJ, Gould MK, Arenberg DA, et al. Management of lung nodules and lung cancer screening during the COVID-19 pandemic: CHEST Expert Panel Report. Chest. 2020;(April), http://dx.doi.org/10.1016/j.chest.2020.04.020, pii:S0012-3692(20)30758-3.

31.Wahidi M.M., Lamb C., Murgu S., et al. March 19th, 2020 Update to the American Association for Bronchology and Interventional Pulmonology (AABIP) Statement on the Use of Bronchoscopy and Respiratory Specimen Collection in PatientswithSuspected orConﬁrmed COVID-19Infection. https://aabronchology.org/wp-content/uploads/2020/03/AABIP-State ment-on-Bronchoscopy-COVID3-12-2020-Statement-plus-3-19-2020 -updates-V3.pdf(accessedon15thJune2020).

32.WuZ,McGooganJM.Characteristicsofandimportantlessons from the coronavirus disease 2019 (COVID-19) outbreak in China: summary of a report of 72 314 cases from the Chinese Center for Disease Control and Prevention. Jama. 2020;323(13):1239---42.

33.DingQ,LuP,FanY,etal.Theclinicalcharacteristicsof pneu-moniapatients co-infected with 2019 novelcoronavirus and inﬂuenza virus in Wuhan, China. J MedVirol. 2020;(March), http://dx.doi.org/10.1002/jmv.25781.

34.Hellyer TP, McAuley DF, Walsh TS, et al. Biomarker-guided antibioticstewardshipinsuspectedventilator-associated pneu-monia(VAPrapid2):arandomisedcontrolledtrialandprocess evaluation.LancetRespirMed.2020;8(2):182---91.

35.Biselli P,FrickeK, Grote L, et al. Reductions indead space ventilationwithnasalhighﬂowdependonphysiologicaldead spacevolume:metabolic hoodmeasurementsduringsleepin patients with COPD and controls. Eur Respir J. 2018;51(5): 1702251.

36.BatraH,YannusL.Indicationsandcomplicationsofrigid bron-choscopy.ExpertRevRespirMed.2018;12(June(6)):509---20. 37.PathakV,WelsbyV,MahmoodK,etal. Ventilationand

anes-theticapproachesforrigidbronchoscopy.AnnAmThoracSoc. 2014;11(May(4)):628---34.

38.PitiotV,GrallM,PloinD,etal.TheuseofCT-scaninforeignbody aspirationin children:a6 years’experience.Int.J.Pediatr. Otorhinolaryngol.2017;102:169---73.

39.AhmedOG,GuillermanRP,GiannoniCM.Protocolincorporating airwayCTdecreasesnegativebronchoscopyratesforsuspected foreignbodiesinpediatricpatients.IntJPediatr Otorhinolaryn-gol.2018;109:133---7.

40.YarmusL, Feller-KopmanD.New bronchoscopic instrumenta-tion: a review and update inrigid bronchoscopy. In:Beamis JF, Mathur PN,Mehta AC,editors. Interventional pulmonary medicine.Lungbiology inhealthanddisease230.NewYork: InformaHealthcare;2010.p.1---9.

41.Zhu J, Zhong Z, Li H, et al. CT imaging features of 4,121 patientswith COVID-19: a meta-analysis.JMed Virol. 2020, http://dx.doi.org/10.1002/jmv.25910[Epubaheadofprint]. 684 685 686 687 688 689 690 691 692 693 694 695 696 697 698 699 700 701 702 703 704 705 706 707 708 709 710 711 712 713 714 715 716 717 718 719 720 721 722 723 724 725 726 727 728 729 730 731 732 733 734 735 736 737 738 739 740 741 742 743 744 745 746 747 748 749 750 751 752 753 754 755 756 757 758 759 760 761 762 763 764 765 766 767 768 769 770 771 772 773 774 775 776 777 778 779 780 781 782 783 784 785 786 787 788 789 790 791 792 793 794 795 796 797 798 799 800 801 802 803 804 805 806 807 808 809 810 811 812 813 814 815 816

(12)

42.Salehi S,Abedi A,BalakrishnanS, et al.Coronavirusdisease 2019(covid-19):asystematicreviewofimagingﬁndingsin919 patients.AJRAmJRoentgenol.2020;(March):1---7.

43.Lin C, Ding Y, Xie B, Sun Z, Li X, Chen Z, et al. Asymp-tomaticnovelcoronaviruspneumoniapatientoutsideWuhan: thevalueofCTimagesinthecourseofthedisease.ClinImaging. 2020;63:7---9.

44.ChenN, ZhouM,Dong X, etal. Epidemiological and clinical characteristicsof99casesof2019novelcoronaviruspneumonia inWuhan,China:adescriptivestudy.Lancet.2020;(January). S0140-6736(20)30211-30217.

45.Sun R, Liu H, Wang X. Mediastinal emphysema, giant bulla, and pneumothorax developed during the course of covid-19 pneumonia. Korean J Radiol. 2020;(March), http://dx.doi.org/10.3348/kjr.2020.0180 [Epub ahead of print].

46.Aiolﬁ A, Biraghi T, Montisci A, et al. Management of per-sistentpneumothorax withthoracoscopyand blebs resection in covid-19 patients. Ann Thorac Surg. 2020;(April). S0003-4975(20)30604-4.

47.PengQ,WangX,ZhangL.Findingsoflungultrasonographyof novelcoronaviruspneumoniaduringthe2019---2020epidemic. IntensiveCareMed.2020;46(May(5)):849---50.

48.Recomendac¸ões da Sociedade Portuguesa de Pneumologia e do Grupo de Estudos de Cancro do Pulmão na abordagem dos doentes com Cancro do Pulmão durante a Pandemia de COVID-19. https://www.sppneumologia.pt/uploads/ subcanaisconteudosﬁcheiros/orientacoes-da-ct-de-pneumologia-onco logica-da-spp-no-cancro-do-pulmao-durante-a-pandemia-de-covid-19. pdf(accessedon15thJune2020).

49.Hallifax R., Wrightson J.M., Bibby A., et al. Pleural ser-vicesduringtheCOVID-19Pandemic.BritishThoracicSociety.

https://www.brit-thoracic.org.uk/about-us/covid-19-information-for-the -respiratory-community(accessedon15thJune2020).

50.Centers for Disease Control and Prevention. Healthcare Infection Prevention and Control FAQs for COVID-19.

https://www.cdc.gov/coronavirus/2019-ncov/hcp/infection-control-faq. html(accessedon15thJune2020).

51.Society of Interventional Radiology. Aerosol Generating Procedures Performed by Interventional Radiology Clinical Notiﬁcation from the Society of Interventional Radiol-ogy. https://www.sirweb.org/practice-resources/covid-19 -resources/covid-19-clinical-notiﬁcation-3-26-20 (accessed on 15thJune2020). 817 818 819 820 821 822 823 824 825 826 827 828 829 830 831 832 833 834 835 836 837 838 839 840 841 842 843 844 845 846 847 848 849 850 851 852 853 854 855 856 857 858 859