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w w 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

Original

article

Relationship

between

climatic

factors

and

air

quality

with

tuberculosis

in

the

Federal

District,

Brazil,

2003–2012

Fernanda

Monteiro

de

Castro

Fernandes

a,∗

,

Eder

de

Souza

Martins

b

,

Daniella

Melo

Arnaud

Sampaio

Pedrosa

a

,

Maria

do

Socorro

Nantua

Evangelista

a

aUniversidadedeBrasília(UNB),ProgramadePós-graduac¸ãoemEnfermagem,Brasília,DF,Brazil

bUniversidadedeBrasília(UNB),ProgramadePós-graduac¸ãoemGeografia,Brasília,DF,Brazil

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received3July2016 Accepted27March2017 Availableonline23May2017

Keywords:

Tuberculosis Seasonality Airpollution

a

b

s

t

r

a

c

t

Introduction:DespitethehighrateoftuberculosisindicatorsinBrazil,theFederalDistrict

showsalowprevalenceofthedisease.

Objective:Toanalyzetherelationshipbetweenclimaticfactorsandairqualitywith

tubercu-losisintheBrazilianFederalDistrict.

Methodology:Thiswasanecologicalanddescriptivestudycomparing3927newcasesof

TuberculosisregisteredattheFederalDistrictTuberculosisControlProgramwithdatafrom theNationalInstituteofMeteorology,BrazilianInstituteofGeographyandStatistics, Brazil-ianAgriculturalResearchInstitute,BrasiliaEnvironmentalInstitute,andtheFederalDistrict PlanningCompany.

Results:From2003to2012,therehasbeenahigherincidenceofTuberculosis(27.0%)inmale

patientsinthewinter(27.2%).Patientsunder15yearsofage(28.6%)andolderthan64years (27.1%)weremoreaffectedinthefall.Foryouthandadults(15–64years),thehighestnumber ofcaseswasreportedduringwinter(44.3%).Thediseasewasprevalentwithultraviolet radiationover17MJ/m2(67.8%;p=<0.001);relativehumiditybetween31.0%and69.0%(95.8%

ofcases;p=<0.00);12hofdailysunlightormore(40.6%;p=0.001);andtemperaturesbetween 20◦Cand23◦C(72.4%;p=<0.001).InthecityofTaguatingaandsurroundingarea,pollution levelsdroppedto15.2%between2003and2012.Smokelevelsdecreasedto31.9%.Inthe Sobradinhoregion,particulatematterdroppedto13.1%andsmoketo19.3%,coinciding withthereductionofTuberculosisincidenceratesduringthesameperiod.

Conclusion: TheresultsshouldguidesurveillanceactionsforTuberculosiscontroland

elim-inationandindicatetheneedtoexpandobservationtimetonewclimateindicatorsandair quality.

©2017SociedadeBrasileiradeInfectologia.PublishedbyElsevierEditoraLtda.Thisisan openaccessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/licenses/ by-nc-nd/4.0/).

Correspondingauthor.

E-mailaddress:fcastrojuju@gmail.com(F.M.Fernandes). http://dx.doi.org/10.1016/j.bjid.2017.03.017

1413-8670/©2017SociedadeBrasileiradeInfectologia.PublishedbyElsevierEditoraLtda.ThisisanopenaccessarticleundertheCC BY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/).

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Introduction

AlthoughBrazilisamongthe22countrieswiththehighest TBburden(35.4/100,000inhabitants),the BrazilianMidwest Region (MW) presents a low-tuberculosis burden scenario (24.1/100,000inhabitants).TheFederalDistrict(FD)features13 casesper100,000inhabitantsandanannualdecreaseof2.2%, indicatingatrendtowardpre-eliminationofthedisease.1

Sociallimitations,2vitaminDdeficiency,3–6comorbidities,7

and limited access to health services8 are risk factors for

developingTB.In addition,ecological studies conductedin countrieswheretheincidenceofTBwashighrelatethe mag-nitude ofTBto climaticsummer factors –Spain9,10;Peru3;

India10,11;CapeTown,SouthAfrica12;UnitedKingdom,Wales

and Scotland4,10,13; and South Africa, Kuwait, Ireland and

Mongolia.10 InHongKong,TBreportswerehighin

sputum-smearorculturepositivepatientsinthesummer.10,14TBcases

increasedinspringinNewYork15andintherainyseasonin

Cameroon.16InJapan,theseasonalityofTBvariedaccording

toclinicalformandage, beinghigherinthe springamong AFB+ganglionarTByoungpatients(latespringtosummer) andinAFB+elderlyinsummer.17InCapeTown,SouthAfrica,

TBaffectedmorechildreninthespring,12whereasinSpain

wasinthewinter.18Inaddition,studiesrevealedthattheless ultravioletlightexposure,themorefrequentisTB,asverified inAustralia5,19becauseofvitaminDdeficiency.20Incontrast,

inPeruthedevelopmentofTBwashigherinthesummerdue totherainyperiodwithlowsunlightincidence.3

Otherclimaticfactorssuchastemperature,21precipitation,

andhumiditycaninfluencethedevelopmentofMycobacterium

tuberculosis.22 Air quality is affected by atmospheric

pollu-tion,wherecarbonmonoxideinducesbacillaryreactivation23

and increases the incidence of tuberculosis.24 In addition,

largeseasonalamplitudesofTBoftenoccurinuplandregions withtemperate mountainclimate and low annual average temperature.21 Therefore, findings described in the

litera-tureconfirm the relevanceofconducting astudy to better understand how climate and air quality can influence TB developmentintheFederalDistrict.Theobjectiveofthisstudy wastoanalyzetherelationshipbetweenclimaticfactorsand airqualitywithtuberculosisintheFederalDistrictofBrazil (2003–2012).Throughthisanalysis,wesuggestimprovements intheaccuracyofthe monitoringsystemand inthe plan-ningandallocationofresourcestoactivitiesoftheTBcontrol program,takingintoconsiderationtheglobalclimatechange context.

Methodology

ThestudywasconductedintheFederalDistrict(FD),the cap-italcityofBrazil,locatedintheMidwestregion.TheFDhas anareaof5,778,999km2 andisdividedinto 31 administra-tiveregions25(AR),withthehealthsectordistributedinto15

HealthDistricts. Thepublicserviceisresponsible for79.9% ofallhealth actions26 and isthe onlyentitytoprovide TB

treatment.

TheFDhasapopulationof2,957,954inhabitants,2596.6%

ofwhom are livinginurbanareas.26 High-altitude tropical

climateprevailsintheregion,withwetandrainysummers, dry andcoldwinters,and relativehumidityof≤20.0%.The average annual temperatureis 21◦C,with anaverage high of 35.8◦C and an averagelow of16◦C.From 2003 to2012, solar ultraviolet radiation inthe FD showed a variationof 17–20MJ/m2.27Theregionhaslittlecloudinessandan

aver-age75.0%daysofsunshineduringtheyear.Duringtheperiod analyzedinourstudy,ingeneralairqualityinthe FDwas consideredgood.28

Weanalyzed3927TBcases(pulmonary,extrapulmonary, andpulmonary+extrapulmonary)ofpatientsintheFD reg-istered under the information system of health events (SINAN/TB),part ofthe FederalDistrictHealth Department (DF).Weexcludednon-residentsandcaseswithoutaddress identification (0.4%excluded).Health Centersinthe FDare 70.0% publicand free-of-charge,1 and67.3% ofthe Centers

managetuberculosiscases.1

Weanalyzedclimatevariables,airqualityindicators,and demographic data from 2003 to 2012. Secondary data was obtainedfromtheNationalInstituteofMeteorology–INMET,29

Brazilian Agricultural Research Corporation – EMBRAPA,27

BrasiliaEnvironmentalInstitute–IBRAN,28BrazilianInstitute

ofGeographyandStatistics–IBGE,25andtheFederalDistrict

PlanningCompany–CODEPLAN.30

Thevariablesincludeddemographicdata(gender,age, edu-cational level, and race/skin color), climate (temperature), solar radiation levels, relative humidity, and TBincidence. Regarding air qualityand pollution, four regionsinthe FD wereanalyzed:Taguatinga,Sobradinho,theNorthWing,and theSouthWing.Pollutionmonitoringsamplingpointswere definedbyIBRANinordertoprioritizeareaswithhightraffic andpopulationdensity.

Acasewasdefinedasdirectsmearand/orcultureproven TBmediumwithhistopathologyconfirmationorclinicaland epidemiological findings suggestive of TB.1 We used the

Köppen classificationmodel31 forclimateanalysis and the

nationalstandardsestablishedbytheCONAMAResolutionfor airqualityassessment(No.3of28,1990).28

Statistical analyseswere performedusingPearson’s chi-square test to check the dependence or independence of the variables32 with a5%significancelevel. Thestudy was

approvedbytheEthicsCommitteeoftheUniversityofBrasilia, OpinionNo.1,098,421.

Results

The FederalDistrictHealth Department reported4017new casesofTBtoSINAN-TBbetween2003and2012.Outofthe 4017casesatotalof3927wereselected;0.4%excluded:52had no addressinformationand38 forbeing residentsofother states.

Amongthedemographicvariables,therewasa predomi-nanceofmales(63.6%ofcases).Themostfrequentagegroup was15–64years(53.7%),themostcommonlevelofeducation was primaryschool(40.2%), andthepredominantracewas mulatto(44.0%)(Table1).

Inthe10yearsexamined,thehighestincidenceof tubercu-losiswasinthewinter(27.0%),followedbyfall(25.0%),spring (24.7%), and summer (23.3%). Male patientsshowed higher

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Table1–Demographiccharacteristicsofnewcasesoftuberculosisperseasonfrom2003to2012.FederalDistrict,Brazil.

Variables Seasons Total

Spring Summer Fall Winter

n % n % n % n % n % Sex Male 643 25.8 572 22.9 602 24.1 680 27.2 2497 63.6 Female 337 23.6 343 24.0 382 26.7 368 25.7 1430 36.4 Agegroup <15years 42 26.1 33 20.5 46 28.6 40 24.8 161 4.1 15–34years 368 26.2 320 22.8 337 24.0 378 26.9 1403 35.7 35–64years 476 24.6 456 23.5 486 25.1 520 26.8 1938 49.4 65orolder 94 22.1 106 24.9 115 27.1 110 25.9 425 10.8 Race/skincolor White 354 26.2 261 19.3 345 25.5 390 28.8 1350 34.3 Black 92 20.7 90 20.3 104 23.4 157 35.4 443 11.2 Yellow 13 20.6 9 14.2 24 38.0 17 26.9 63 1.6 Mulatto 398 23.0 362 20.9 470 27.1 499 28.8 1729 44.0 Indigenous 3 17.6 3 17.6 5 29.4 6 35.2 17 0.4 Unknown – – – – – – – – 325 8.2 Education Illiterate 54 29.0 41 22.0 48 25.8 43 23.1 186 4.7 Elementary 383 24.3 368 23.3 398 25.2 428 27.1 1577 40.2 HighSchool 193 26.3 159 21.7 193 26.3 188 25.6 733 18.7 University 95 27.2 74 21.2 79 22.6 101 28.9 349 8.9 Unknown – – – – – – – – 1082 27.6

Table2–Climaticconditionsperseasonduringthestudyperiodof2003–2012.FederalDistrict,Brazil.

Variables Seasons Total p-Valuea

Spring Summer Fall Winter

n % n % n % n % n % Temperature <20◦C 66 10.5 58 9.2 177 28.3 324 51.8 625 15.9 20–23◦C 661 23.3 780 27.5 792 27.9 600 21.1 2833 72.1 <0.001 24◦Cormore 253 53.9 77 16.4 15 3.1 124 26.4 469 11.9 Radiation <11MJ/m2 102 44.3 66 28.6 49 21.3 13 5.6 230 5.8 11–16MJ/m2 265 26.4 254 25.3 302 30.1 182 18.1 1003 25.5 <0.001 ≥17MJ/m2 613 22.7 595 22.0 633 23.4 853 31.6 2694 68.6 Humidity ≤30% 26 55.3 0 0.0 1 2.1 20 42.5 47 1.1 31–69% 377 20.2 122 6.5 408 21.8 958 51.3 1865 47.4 <0.001 ≥70% 577 28.6 793 39.3 575 28.5 70 3.4 2015 51.3 Pollutants Smokemg/m3 NorthWing 132.2 20.7 175 27.5 184.4 28.9 144.6 22.7 636.2 25.6 SouthWing 15.4 24.1 15.3 24.1 7.5 12.0 23.8 38.7 62 2.4 <0.001 Taguatinga 188.3 19.2 328.6 33.6 214.3 21.9 244 25.0 975.2 39.2 Sobradinho 92.6 11.4 75.6 9.3 109 13.4 531.3 65.7 808.5 32.5 TSPmg/m3 NorthWing 152.7 21.9 119 17.2 182.1 26.3 237.2 34.2 691 19.2 SouthWing 68.8 23.8 93.9 32.5 53.2 18.3 73.2 25.2 289.1 8 <0.001 Taguatinga 282.1 29.0 256 26.3 175.5 18 257.2 26.4 971 27 Sobradinho 266.2 16.1 278.5 16.8 555.7 33.7 545.5 33.1 1646 45.7

TSP,totalsupendedparticulatematter.

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Table3–Characteristicsofairqualityperseasonduringthestudyperiodof2003–2012.FederalDistrict,Brazil.

Variables Seasons Total p-Valuea

Spring Summer Fall Winter

n % n % n % n % n % Pollutants Smokemg/m3 NorthWing 132.2 20.7 175 27.5 184.4 28.9 144.6 22.7 636.2 25.6 SouthWing 15.4 24.1 15.3 24.1 7.5 12.0 23.8 38.7 62 2.4 <0.001 Taguatinga 188.3 19.2 328.6 33.6 214.3 21.9 244 25.0 975.2 39.2 Sobradinho 92.6 11.4 75.6 9.3 109 13.4 531.3 65.7 808.5 32.5 TSPmg/m3 NorthWing 152.7 21.9 119 17.2 182.1 26.3 237.2 34.2 691 19.2 SouthWing 68.8 23.8 93.9 32.5 53.2 18.3 73.2 25.2 289.1 8 <0.001 Taguatinga 282.1 29.0 256 26.3 175.5 18 257.2 26.4 971 27 Sobradinho 266.2 16.1 278.5 16.8 555.7 33.7 545.5 33.1 1646 45.7

TSP,totalsupendedparticulatematter.

a p-Value=Pearson’schi-squaretestwitha5%significance.

incidenceinwinter(27.2%)and femalesin thefall(26.7%). Therewasahigherincidenceininfantsandchildrenunder15 yearsinthefall(28.6%).Youthandadults(15–64yearsofage) becameillmoreofteninthewinter(44.3%)whilepatientsover 64yearsinthefall(27.1%)(Table1).

ConsideringclimatevariablesintheFD,tuberculosiswas more prevalent with ultraviolet radiation conditions (UVR) above17MJ/m2(67.8%;p=<0.001);relativehumiditybetween 31.0%and69.0%(95.8%;p=<0.001);precipitationvaluesless than1mm(71.7%;p=<0.001);dailysunlightexposureover12h (40.6%; p=0.001); and temperaturebetween 20◦C and 23◦C (72.4%;p=<0.001)(Table2).

Inrelation toair quality, the two mainpollutants were smoke (CO2, CO, SO2 and NO2) and total suspended par-ticulate matter (TSP). Among the regions covered by the study(Taguatinga,Sobradinho,NorthWing,andSouthWing), pollutionlevelswerethehighestinTaguatingaand Sobrad-inhoregions,bothwithhazardouslevels ofhealthconcern –TSP≥375mg/m3 andsmoke250mg/m3. Weidentified a greater amount of pollutants in the spring in Taguatinga region (38.5%), and in the winter in Sobradinho (50.0%) (Table3).DuringthestudyperiodadropofTSPandsmoke rates inTaguatinga (−15.2%and −31.9%, respectively)was observed.Similarly,TSPandsmokelevelsreducedin Sobrad-inho (−13.1% and −9.3%, respectively). These decreases in pollutionandsmokelevelswereassociatedwithlower inci-dencerates(IR)ofTBinthesameperiod,withareductionof 46%inTaguatingaandof66.5%inSobradinho.Thesefindings suggestthatthedecreaseofpollutantswasassociatedwith thereductionofTBcasesintheregion.

Discussion

Regardingthedemographicprofile,thehighestincidenceof TBintheFDoccurredinyoungadultmalepatients,with ele-mentaryeducation,andofmulattorace.Likewise,67.0%ofthe BrazilianTBpatientswereyoungadultmales.1InCameroon,

TB was significantly more prevalent in males (12.6%)

comparedtofemales (10.7%).16Peru,3 China,23 Spain,18 and

theUnitedStates21showedsimilarresults.

Inthepresentstudy,thehighestincidenceofcasesin chil-drenunder15yearsofageintheFDoccurred inthefall,a seasoncharacterizedbymildtemperaturesandlongperiods without rain. Theresult is similar tothat reported in the UnitedStates,wheretherewasapeakofchildhoodTBfrom springtolatefall.21Thestudiessuggestaseasonintervalfor

thetransmissionofTBfromadultstochildrensince,in gen-eral,childhoodTBpeaksinthenextseasonfollowingadultTB peak.12Youthandadults(15–64yearsofage)developmoreTB

inthewinter(53.7%)andpatientsover64inthefall(27.1%). ThisissomewhatsimilartowhathappenedinChina,where the incidencewas 15.7% inchildrenunder15 years ofage and 34.0% inthe age range of 15–64years, predominantly duringthewinterandfall.33Inthisstudy,childrenunder15 years of age developed less TB,despite their physiological disadvantages,suchasdecreasedcardiacoutput,accelerated metabolism,developingimmunesystem,andotherformsof age-leveldevelopmentalcharacteristics.34OutofTBpatients

inChina50.3%wereolderthan64,wherelifeexpectancyis 75.7years.33SimilareventswereobservedinJapan,4United

Kingdom14andtheUnitedStates,21 wherelifeexpectancies

were83,81,and78years,respectively.

Severalauthorsunderscoreanassociationofloweducation level andTB.2,35,36 Onestudy inSpainindicatedthat 53.8%

ofthe patients had notcompletedprimary education.37 In

China,38 patients withlessthan sixyearsofschooling had

ariskofrelapse3.4timeshigher,andariskofdefaulting4.3 timesgreaterinnewlytreatedTBcases.IntheFD,TBwasmore prevalentintheleasteducatedgroup(<8yearsofeducation; 44.9%),reinforcingtheassociationoflowerlevelofeducation andthedisease,highlightingthat27.6%oftheresponseswere ignored.ConsideringraceinBrazil,25mulattowasthemost

frequentraceseeninTBpatientsoftheFD.

SeasonalityanalysisrevealedthatTBwasmoreprevalent inthewinterintheFD,similarlythatobservedinotherregions ofthecountry.39IntheUnitedKingdom,4reducedsun

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tuberclebacillusbecauseofvitaminDdeficiency. Tempera-turesinthewinterintheMidwestregionofBrazilvaryfrom 12◦Cto27◦C.ItisworthnotingthatinBrazilthefour sea-sonsarenotmarkedlydifferentastheyareinotherregionsin theworld.AseasonalpatternofTBwithapredominantpeak duringthefallwasobservedintheFD.Asimilarpatternwas verifiedinPeru,3wherethediagnosisoftuberculosisincreases

inlatesummerandearlyfallbecauseoftherainy character-isticsofthoseseasons.Highhumidityandabsenceofdirect sunlightduetocloudinessaresimilarcharacteristicsofthe Brazilianautumn.

A high level of UV radiation was observed in the FD, averaging17MJ/m2with12h/dayofincidentsunlight(40.6%;

p=0.001).Thisprobablyoccursduetogeographicalaspectsof theFD–plateaureliefwithsmoothtopography–that facili-tatethepenetrationofsunlight.Thisfactshouldjustifythe lower TB incidence rates in the region compared to other areas ofthecountry.1 TB incidencepeaksin the winterin

Perucoincidewiththelowsunlightperiodsduetovitamin Ddeficiency.3,5,6,40,41InEngland,13lowlevelsofvitaminDin

post-wintermightresultinanimpairmentofcellular immu-nityleadingtoreactivationofmycobacterialinfectionaftera periodoflatency.

IntheFD,95.8%ofTBcasesoccurredwithrelative humid-ity between 31.0% and 69.0% and precipitation values less than1mm(71.7%;p=<0.001).ItisnoteworthythatEuropean humidityishigh(70.0%average)duetohighrainfallcaused bywindsthatbringmoisturefrom the oceantothe conti-nentalmostallyearround.4InCameroon,moreTBcaseswere

recordedintherainyseason,withasignificantdifferenceas comparedtootherseasons.16Similarly,agreaterincidenceof

TBinMongoliaoccursinwetseasons.22

Possibleexplanationsforseasonalvariationsinthe inci-denceofTBincludedecreasedvitaminDlevelsinwinter,6,40–42

whichleadstodepressionofimmuneresponseand conse-quentreactivationofTB.AnotherriskfactorforTBinwinter ishouseholdcrowding,15whichmaybefoundinthepoorest

areasintheFD.Itisnoteworthythatdirectsunlightispresent during75.0%ofthedaysintheFD.29Highsolarradiationmay

explainthelowerincidenceoftuberculosisintheregion com-paredtootherareasofthecountry.

MorecasesofTBwerereportedintheFDwhenthe tem-peraturewasbetween20◦Cand23◦C(72.4%ofcases),inline withseveralstudies carried outin differentplaces, includ-ing:NewYork(20–25◦C)15;Spain(16–24C)9;CapeTown,South

Africa(13–23◦C)41;UK(11.7Cand21.1C)4;andPeru.3

How-ever, TB was also diagnosedat higher temperatures: 39◦C in Cameroon16; 21–39C in Northern India11; and 20–38C in Kuwait.43 Lower temperatures have been identified in

Japan(5◦C)44 and Mongolia (−5Cto9C).22 In general,TB

incidenceswerehigherinmildertemperatures,similarto con-ditionsreportedintheFD.

Inrelationtoairquality,twomainpollutantswere iden-tified inthe FD: smoke (CO2, CO, SO2, and NO2)and total suspendedparticulatematter(TSP),especiallyinTaguatinga andSobradinho.InSobradinhoTBnotificationswerehigher inwinter;inTaguatingainspring.Althoughthe FDhas15 health districts, onlyfour points could be sampled for air qualityanalysis:theSouthWing,theNorthWing,Taguatinga, andSobradinho. Itisimportanttomentionthatairquality

improvedintheFDasaresultofaResolution(CONAMANo. 242/1998)thatregulatesmodesoftransportationandactions issuedbytheNationalCouncilfortheEnvironmentto con-trolairquality(providedinCONAMAResolutionNo.436/2011 prohibitingtheemissionofpollutantsinthefederalcapital byindustries).Despitethelimitationofairqualitymonitoring equipmentintheFD(onlyfour),thedataseemtoindicatethat airpollutionisdirectlyrelatedtoTBincidence.Studiesinthe USandRussiaalsosuggestalinkbetweenconcentrationsof smokeandtotalsuspendedparticulatematterand tuberculo-sis,especiallyconsideringtheamountsofNO2andCO2.24,45 AirpollutiongeneratedbytrafficinTaiwan–causedby sul-fur dioxide, ozone, and carbon monoxide– wasassociated withculture-confirmedTB.46Likewise,astudyinSouthKorea

revealedthatlong-termexposuretoambientSO2increased theriskofTBby7.0%inmales.47

In this study, Taguatinga and Sobradinho showed lev-els of greathealth concern;i.e., TSPpollution ≥375mg/m3 andsmoke≥250mg/m3.Ahigheramountofpollutantswas reportedinTaguatinga(38.5%)inspringandinSobradinhoin winter(50.0%).InSouthKorea,theexposuretohigh concen-trationsofsuspendedparticlesintheatmosphereincreased at1.27timestheincidenceofTB48andtheexposuretofine

particulate matter (PM 2.5) was associated with increased riskofthedisease.49 InTaiwan,exposuresuspended

parti-clesincreasedtherateofTBby4.0%andinterferedwithsmear results.Thechronicexposureto≥50␮g/m3PM10mayprolong thesputumcultureconversionofTBpatientswith sputum-positiveculture.38

Amongthelimitationsofthestudyistheuseofsecondary bases ofSINAN-TB sincethe information can be inconsis-tentduetoincompleterecordsand/ormissingdataleadingto methodologicalbias.Otherlimitationswerethelackofmore effectiveairpollutionassessmentsindifferentregionsofthe FDandtheanalysisofairqualityrestrictedtosmokeandto certainparticulatematter.

Insummary,theresultssuggestthattheincidenceofTB appearstohavebeenaffectednotonlybyclimaticfactors– seasonsandclimaticvariables,solarradiation,temperature, humidity,andairquality–butalsobysocialanddemographic factors–age,gender,race,andeducation.However,we under-scorethe needforfurtherstudies sothat therole ofother environmental variables can beclarified. Air-quality obser-vationtimeshould alsobeincreasedsothatwecanbetter understandtherelationshipofTBwiththeweather.

Conflicts

of

interest

Theauthorsdeclarenoconflictsofinterest.

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