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
aaUniversidadedeBrasília(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
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b
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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/).
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
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.
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 andsmoke≥250mg/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
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(16–24◦C)9;CapeTown,South
Africa(13–23◦C)41;UK(11.7◦Cand21.1◦C)4;andPeru.3
How-ever, TB was also diagnosedat higher temperatures: 39◦C in Cameroon16; 21–39◦C in Northern India11; and 20–38◦C in Kuwait.43 Lower temperatures have been identified in
Japan(5◦C)44 and Mongolia (−5◦Cto9◦C).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≥50g/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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s
1.MinistériodaSaúde(BR).SecretariadeVigilânciaemsaúde. BolEpidemiol.2016;47:13.
2.VianaPVS,Gonc¸alvesMJF,BastaPC.Ethnicandracial inequalitiesinnotifiedcasesoftuberculosisinBrazil.PLOS ONE.2016;11.
3. WingfieldT,SchumacherSG,SandhuG,etal.Theseasonality oftuberculosis,sunlight,vitaminD,andhouseholdcrowding. JInfectDis.2014;210:774–83.
4. KohGCKW,HawthorneG,TurnerAM,KunstH,DedicoatM. Tuberculosisincidencecorrelateswithsunshine:an ecological28-yeartimeseriesstudy.PLOSONE.2013;8. 5. MaclachlanJH,LavenderCJ,CowieBC.Effectoflatitudeon
seasonalityoftuberculosis,Australia,2002–2011.EmergInfect Dis.2012;18:1879–81.PMID:23092594.
6. VisserDH,SchoemanJF,VANFurthAM.Seasonalvariationin theincidencerateoftuberculousmeningitisisassociated withsunshinehours.EpidemiolInfect.2013;141:459–62. PMID:22647556.
7. FoxGJ,BarrySE,BrittonWJ,MarksGB.Contactinvestigation fortuberculosis:asystematicreviewandmeta-analysis.Eur RespirJ.2012;41:140–56.
8. SouzaMSPL,AquinoR,PereiraSM,etal.Fatoresassociados aoacessogeográficoaoservic¸odesaúdeporpessoascom tuberculoseemtrêscapitaisdoNordestebrasileiro.Cad SaudePublica.2015;31:111–20.
9. LuqueroF,Sanchez-PadillaE,Simon-SoriaF,EirosJM,Golub JE.TrendandseasonalityoftuberculosisinSpain,1996–2004. IntJTubercLungDis.2008;12:221–4.PMID:18230258. 10.FaresA.Seasonalityoftuberculosis.JGlobInfectDis.
2011;3:46–55.
11.ThorpeLE,FriedenTR,LasersonKF,etal.Seasonalityof tuberculosisinIndia:isitrealandwhatdoesittellus? Lancet.2004;364:1613–4.
12.SchaafHS,NelED,BeyersN,etal.Adecadeofexperience withMycobacteriumtuberculosisculturefromchildren:a seasonalinfluenceonincidenceofchildhoodtuberculosis. TuberLungDis.1996;77:43–6.
13.DouglasAS,AliS,BakhshiSS.DoesvitaminDdeficiency accountforethnicdifferencesintuberculosisseasonalityin theUK?EthnHealth.1998;3:247–53.
14.LeungCC,YewWW,ChanTY,etal.Seasonalpatternof tuberculosisinHongKong.IntJEpidemiol.2005;34:924–30. 15.ParrinelloCM,CrossA,HarrisTG.Seasonalityoftuberculosis
inNewYorkCity,1990–2007.IntJTubercLungDis. 2012;16:32–7.
16.Ane-AnyangweIN,AkenjiTN,MbachamWF,PenlapVN, TitanjiVP.Seasonalvariationandprevalenceoftuberculosis amonghealthseekersintheSouthWesternCameroon.East AfrMedJ.2006;83:588–95.
17.NagayamaN,OhmoriM.Seasonalityinvariousformsof tuberculosis.IntJTubercLungDis.2006;10:1117–22. 18.RiosM,GarciaJM,SanchezJA,PerezD.Astatisticalanalysis
oftheseasonalityinpulmonarytuberculosis.EurJEpidemiol. 2000;16:483–8.
19.RalphAP,LucasRM,NorvalM.VitaminDandsolarultraviolet radiationintheriskandtreatmentoftuberculosis.Lancet InfectDis.2013;13:77–88.
20.JeevanA,SharmaAK,McMurrayDN.Ultravioletradiation reducesresistancetoMycobacteriumtuberculosisinfection. Tuberculosis(Edinb).2009;89:431–8.
21.WillisMD,WinstonCA,HeiligCM,CainKP,WalterND, MacKenzieWR.SeasonalityoftuberculosisintheUnited States,1993–2008.ClinInfectDis.2012;54:1553–60.
22.NaranbatN,NymadawaP,SchopferK,RiederHL.Seasonality oftuberculosisinanEastern-Asiancountrywithanextreme continentalclimate.EurRespirJ.2009;34:921–5.
23.TremblaGA.Historicalstatisticssupportahypothesislinking tuberculosisandairpollutioncausedbycoal.IntJTuberc LungDis.2007;11:722–32.
24.ShilovaMV,GlumnaiaTV.Influenceofseasonaland
environmentalfactorsontheincidenceoftuberculosis.Probl TuberkBoleznLegk.2004:17–22.
25.InstitutoBrasileirodeGeografiaeEstatística.Censo Demográfico2010.Característicasdapopulac¸ãoedos domicílios:resultadosdouniverso.RiodeJaneiro:IBGE;2016. Availablefrom:http://www.ibge.gov.br/home/estatistica/ populacao/censo2010/característicasdapopulacao/ resultadosdouniverso.pdf
26.CohnA,organizador.Questionandoconceitos:opúblicoeo privadonasaúdenoséculo21.In:CohnS,RodriguesN, AmaranteP.Gestãopúblicaerelac¸ãopúblicoprivadona saúde.RiodeJaneiro:Cebes;2010.p.324.
27.MinistériodaAgricultura,PecuáriaeAbastecimento(BR). Estac¸õesclimáticas.EMBRAPA;2015.
28.InstitutoBrasíliaAmbiental.Qualidadedoar,relatórios anuaisdemonitoramento.IBRAN;2012.
29.MinistériodaAgricultura,PecuáriaeAbastecimento(BR). InstitutoNacionaldeMeteorologia.INMET;2015.
30.CompanhiadePlanejamentodoDistritoFederal–CODEPLAN, PDAD–PesquisaDistritalporAmostradeDomicílios2015. 31.KoeppenW.Climatologia:conumestudiodelosclimasdela
tierra.Mexico:Fondodeculturaeconomica;1948,478pp. 32.BussabWO,MorettinPA.EstatisticaBásica.8thed.SãoPaulo:
Saraiva;2013.
33.LiX-X,WangL-X,ZhangH,etal.Seasonalvariationsin notificationofactivetuberculosiscasesinChina,2005–2012. PLOSONE.2013;8:e68102.
34.MoriT.Recenttrendsintuberculosis,Japan.EmergInfectDis. 2000;6:566–8.
35.CostaJSD,Gonc¸alvesH,MenezesAMB,etal.Controle epidemiológicodatuberculosenacidadedePelotas,Rio GrandedoSul,Brasil:adesãoaotratamento.CadSaúde Pública.1998;14:409–15.
36.MascarenhasMDM,AraújoLM,GomesKRO.Perfil epidemiológicodatuberculoseentrecasosnotificadosno municípiodePiripiri,EstadodoPiauí,Brasil.EpidemiolServ Saúde.2005;14:7–14.
37.MartinSacnhesV,Alvarez-GuisasolaF,CaylaJA,AlvarezJL. Predictivefactorsofmycobacteriumtuberculosisinfection andpulmonarytuberculosisinprisoners.IntJEpidemiol. 1995;24:630–6.
38.WangJ,ShenH.Reviewofcigarettesmokingandtuberculosis inChina:interventionisneededforsmokingcessation amongtuberculosispatients.BMCPublicHealth.2009;9:292. 39.FrancoJF,MoraesJR,SantanderLAM,etal.Relac¸ãoentrea
ocorrênciadetuberculoseeumconjuntodefatores sócioeconômicos,demográficosedesaúdedapopulac¸ão brasileirausandoaPNAD;2003.
40.Sita-LumsdenA,LapthornG,SwaminathanR,MilburnHJ. ReactivationoftuberculosisandvitaminDdeficiency:the contributionofdietandexposuretosunlight.Thorax. 2007;62:1003–7.
41.MartineauAR,NhamoyebondeS,OniT,etal.Reciprocal seasonalvariationinvitaminDstatusandtuberculosis notificationsinCapeTown,SouthAfrica.ProcNatlAcadSciU SA.2011;108:19013–7.
42.NnoahamKE,ClarkeA.LowserumvitaminDlevelsand tuberculosis:asystematicreviewandmeta-analysis.IntJ Epidemiol.2008;37:113–9.
43.AkhtarS,MohammadHG.Seasonalityinpulmonary tuberculosisamongmigrantworkersenteringKuwait.BMC InfectDis.2008;8:3.PMID:18179720.
44.OnozukaD,HagiharaA.Theassociationofextreme
temperaturesandtheincidenceoftuberculosisinJapan.IntJ Biometeorol.2015;59:1107–14.
45.SmithGS,SchoenbachVJ,RichardsonDB,GammonMD. Particulateairpollutionandsusceptibilitytothedevelopment ofpulmonarytuberculosisdiseaseinNorthCarolina:an ecologicalstudy.IntJEnvironHealthRes.2014;24:103–12.
46.LaiTC,ChiangCY,WuCF,etal.Ambientairpollutionandrisk oftuberculosis:acohortstudy.OccupEnvironMed.
2016;73:56–61.
47.HwangSS,KangS,LeeJY,etal.Theimpactofoutdoorair pollutionontheincidenceoftuberculosisinSeoul metropolitanarea,SouthKorea.KoreanJInternMed. 2014;29:183–90.
48.KimJ.Isambientairpollutionanotherriskfactorof tuberculosis?KoreanJInternMed.2014;29:170–2. 49.LeeSH,HwangED,LimJE,etal.Theriskfactorsand
characteristicsofCOPDamongnonsmokersinKorea:an analysisofKNHANESIVandV.Lung.2016;194:353–61.