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Levels and neurodevelopmental effects of polycyclic aromatic
hydrocarbons in settled house dust of urban dwellings on
preschool–aged children in Nanjing, China
Bing–LingWang
1,Shu–TaoPang
1,Xiao–LingZhang
2,Xi–LingLi
3,Yong–GangSun
4,Xiao–MeiLu
2,
QiZhang
5,Zheng–DongZhang
51 QingdaoCentersforDiseaseControlandPrevention,Qingdao266033,China 2 DepartmentofHygieneAnalysisandDetection,SchoolofPublicHealth,NanjingMedicalUniversity,Nanjing211166,China 3 InstituteofChildHealthCare,NanjingMaternityandChildHealthCareHospital,Nanjing210004,China 4 DepartmentofChildHealthCare,MaternityandChildCareCenterofGulouDistrictofNanjing,Nanjing210029,China 5 DepartmentofOccupationalMedicineandEnvironmentalHealth,SchoolofPublicHealth,NanjingMedicalUniversity,Nanjing211166,China
ABSTRACT
Thisstudyinvestigatedlevelsandpossibledeterminantsofpolycyclicaromatichydrocarbons(PAHs)insettledhousedust of urban dwellings with preschool–aged children in Nanjing, China. The possible neurodevelopmental effects of house– dustPAHsonthechildrenwerealsoinvestigated.Settledhousedustwascollectedfrom203urbanhouses.FifteenPAHs weremeasuredusinganHPLCwithafluorescencedetectorandwavelengthprogramming.TheChildBehaviorChecklist and the Gesell Development Inventory were used to evaluate the overall development of the children. PAHs were detectedinsettledhousedustof>90%ofhouses,wherehighmolecularweightPAHspredominated.MostPAHswithtwo orthreeringswerefoundatsignificantlyhigherlevelsinindoorcomparedwithoutdoordust.PAHisomericratiosshowed thatPAHswithfourormoreringsmightbederivedfromoutdoorcoalburningsources.Naphthalenewasfoundatlower concentrationsinhouseswithmorehoursofnaturalventilation,whilepyrene,chrysene(Chr)andbenzo[k]fluoranthene (BkF) were present at higher concentrations in these houses. A higher floor level correlated with lower levels of PAHs, especially those with four or more rings, while older houses had higher PAH levels. Benzo[a]pyrene (BaP) and indeno[1,2,3–cd]pyrene levels were positively associated with most behavioral problem scores. Higher BaP and benzo[g,h,i]perylene levels showed lower Gesell language development quotient (DQs), and higher Chr and BkF were associated with lower Gesell social skill DQs. In conclusion, 15 PAHs are ubiquitous in urban settled house dust, where outdoorcoalburningandindoorcookingoilfumesarethetwomainsourcesofPAHsinNanjing,China.Naturalventilation, floor level and residence age potentially influence house dust PAH levels. The potential adverse effect of postnatal exposuretoPAHsonthebehaviorandneurodevelopmentofpreschool–agedchildrenrequiresfollowupinlargerstudies. Keywords:Urbanhousedust,polycyclicaromatichydrocarbons,childexposure,neurodevelopment CorrespondingAuthor:Bing-Ling Wang
:+86Ͳ532Ͳ85646110 :+86Ͳ532Ͳ85623909 :wangbl74@gmail.com ArticleHistory: Received:30October2013 Revised:15January2014 Accepted:15January2014 doi:10.5094/APR.2014.0351.Introduction
Concentrations of chemical contaminants, such as semi– volatile organic compounds like polycyclic aromatic hydrocarbons (PAHs),flameretardantsandpesticides,areoftenhigherinindoor air than in outdoor air (Rudel and Perovich, 2009). Many indoor contaminants absorb onto particulate matter, which is initially suspended in air and later settles as dust. This has led to settled housedustbeingconsideredasanexposuremediumandaglobal indicator of residential contamination (Butte and Heinzow, 2002; Lioyetal.,2002),particularlyforinfantsandtoddlers,whoareat highestriskbecauseoftheirhand–to–mouthactivities.
Prenatal PAH exposure has been linked to neurodevelopͲ mental toxicity. For example, maternal PAH exposure during pregnancyhasbeenassociatedwithIQdeficits(Pereraetal.,2009; Edwardsetal.,2010)andcognitivedevelopmentaldelay(Pereraet al., 2006; Edwards et al., 2010). Given that neurodevelopmental processessuchasmyelinationarenotcompleteduntiladolescence (RiceandBarone,2000),andthatinadvertentdustingestioncould beresponsibleforasmuchas42%ofnon–dietaryPAHexposurein youngchildren(Gevaoetal.,2007),settledhousedustmaybean importantsourceofPAHuptakeinchildren.
Studies have reported PAH levels in settled house dust in different localities and countries (Rudel et al., 2003; Maertens et al.,2004;Gevaoetal.,2007;Maertensetal.,2008;Robertsetal., 2009;Langeretal.,2010).However,tothebestofourknowledge, onlyonestudyreportedthePAHfloorloadingsinChina,withonly 14settledhousedustsamplesforsmallruralvillages(Naspinskiet al.,2008).Inthisstudy,PAHconcentrationsinurbansettledhouse dust were measured in Nanjing, China, to evaluate urban indoor PAH pollution, their possible determinants and sources. SimulͲ taneously,thebehaviorandneurodevelopmentofpreschool–aged children in these houses were tested to find any association with thecorrespondingPAHlevels.
2.Methods
2.1.Subjectrecruitment Recruitmentquestionnaires(n=500)weresenttofamilieswith preschool–aged children (4–5 years) randomly selected from the four largest public kindergartens in the Gulou district of Nanjing, China,ofwhich464answeredandreturnedthequestionnaire.The exclusion criteria we used included (1) living in the current house forlessthan1year;(2)birthingproblems,suchasdeliveryinjuries or a low birth weight; (3) neonatal problems, such as asphyxia,
intracranial hemorrhage, hypoxic–ischemic encephalopathy and severe jaundice; (4) acquired disabilities, including poisoning, encephalitis, meningitis, encephalopathy, cerebral trauma and cerebral injuries following convulsions; and (5) developmental dysplasia or other developmental defects influenced by malnuͲ tritionorinheritedmetabolicdiseases.Subjectrecruitmentisalso described elsewhere (Wang et al., 2012). Based on these criteria, 400 preschool–aged children were selected for the house investigation and the measures of behavior and neurodevelopͲ ment.Duringthefieldinvestigation,146familiesoptedoutofthe survey because of the in–house sampling date conflicted or becausetheythoughtthereweretoomanyquestionsinthe113– item Child Behavior Checklist. Of the remaining 254 families, becauseoftheinvasivebloodsampling,only98childrenprovided finger–prick blood and performed the Gesell Development Inventory test (Table 1). Informed consent was obtained from all participants and the Institutional Ethics Committee of Nanjing Medical University and Institutional Review Board approved the study. Table1.Characteristicsofthesubjectsandtheirhouses(n=203) Contents Children'scharacteristics Sex(n(%)males) 104(51) Age(n(%)) 4 100(49) 5 103(51) CBCLscores(n) 203 DQs(n) 98 BloodPblevels(ʅg/L,n=98,) [mean±SD(Min,Max)] 45±15(30,75) Housecharacteristics Residenceage[mean±SD(Min,Max)] 16±8(1,60) Floorlevel[mean±SD(Min,Max)] 5±5(1,28) Frequencyofnaturalventilation[n(%)] <1hr/d 127(63) 1–4hr/d 63(31) >4hr/d 13(6) Smokingstatus[n(%)] No 118(58) Yes 85(42) Neartoamainroad(<500meters) No 99(49) Yes 104(51) Vacuumorwipecleaningfrequency[n(%)] 1–3d 118(58) 4–7d 52(26) 7–14d 21(10) >14d 12(6) Kitchentype[n(%)] Open 61(30) Separate 142(70) 2.2.Buildinginvestigationsanddustsampling
Settled house dust was sampled from the houses of all subjects recruited during the non–heating season from March to June 2011. One sample of dust from each house was collected using commercial vacuum cleaners and paper bags on the floor surfaceineachdwellingwherepreschool–agedchildrencommonly played.Simultaneously,settleddustonanoutdoorgroundsurface
near the housewas sampled with a hand–heldbrush. For further detailsofthesamplingprocess,pleaseseetheSupportingMaterial (SM). In total, 230 samples of indoor settled house dust and 150 outdoor settled dust samples were collected. After excluding mislabeled, mis–stored and insufficient dust samples (26 samples andonesingle–familyhomedustsamplewereexcluded),atotalof 203samplesofindoordustand110pairedoutdoordustsamples from low or high–rise apartment buildings were available for the final analysis. During dust sampling, the caregivers were asked to provide information about residence age, floor level, household smoking,kitchentype(openorseparate)andcookinghabits(once, twice or three times per day), frequency of natural ventilation through open windows (<1hr/d, 1–4hr/d or >4hr/d), vacuum or wipe cleaning frequency (every 1–3d, 4–7d, ч14d or >14d) and whether the residence was near a main road (<500meters from thechild’shometoatwo–ormore–lanemotorway)(Table1).
2.3.PAHlaboratoryanalysis
Pretreatment and laboratory measurements of PAHs in dust were carried out following the method described by Lu et al., (2011). Particles were separated from fibers by sieving through a meshthatwas<150ʅminsize.Acetonewasaddedtoeachsieved dust sample and extraction was performed in an ultrasonic bath. The supernatant was concentrated and then spiked with methyl cyanide to 0.1mL. Using methyl cyanide and water as the mobile phase,PAHswereseparatedbygradientelutionanddetectedwith a fluorescence detector and wavelength programming. Targeted PAHs included: naphthalene (Nap), acenaphthene (Ace), fluorene (Flu), phenanthrene (Phe), anthracene (Ant), fluoranthene (Fla), pyrene (Pyr), benz[a]anthracene (BaA), chrysene (Chr), benzo[b]Ͳ fluoranthene (BbF), benzo[k]fluoranthene (BkF), benzo[a]pyrene (BaP), dibenz[a,h]anthracene (DBA), benzo[g,h,i]perylene (BP) and indeno[1,2,3–cd]pyrene (IP). The fifteen PAHs were efficiently separatedwithin28minandshowedgoodlinearitywithinthe0.5– 50ng/mLrange.Theabsoluterecoveryefficiencieswere62–110% andtherelativestandarddeviation(RSD)rangedbetween1.4and 5.9% (Lu et al., 2011). The instrumental detection limit (IDL) was determined on the basis of response at a signal–to–noise ratio (S/N) of 3. The method detection limits (MDL) under the present chromatographic conditions were calculated using the IDLs, the volumeofextracts,andthesampleweights.
2.4.Measuresofchildbehaviorandneurodevelopment
All 203 children in the houses where dust samples were collected were asked to check their behavioral and neurodevelopmentproblems.Behavioralproblemsweremeasured by caregiver report on the 113–item Child Behavior Checklist (CBCL) for children 4–16 years of age (Achenbach, 1991), which collects information on child behaviors occurring in the past 6 months and has been proved workable in China (Xin and Zhang, 1992). The caregivers completed the CBCL with guidance as needed from the research workers. The syndrome scores were computed for all eight syndrome domains (anxious/depressed, withdrawn/depressed, somatic complaints, social problems, thoughtproblems,attentionproblems,compulsiveandaggressive behavior) by summing the scores on the specific items, yielding a continuousrawscore.Basedonresponsestothesyndromescales, internalizing, externalizing and total problem scores were obtained.
The Gesell Development Inventory has been translated and standardizedbytheBeijingChildren’sHealthCareInstitute,which consists of five behavioral domains: adaptive, gross motor, fine motor, language and personal social behaviors (Zhu et al., 1983). The items used for the five behavioral domains included: (1) adaptive behavior: eye–hand coordination, imitation, object recovery,comprehension,discriminativeperformance,perception, completion and number conception; (2) gross motor behavior: posturalresponses,balanceofthehead,andpostureatstanding,
sitting and walking; (3) fine motor behavior: ability to use hands and fingers to manipulate objects; (4) language behavior: vocabulary, word comprehension, conversation and word production; (5) personal social behavior: reactions to persons, personal habits, initiative and independence, play responses and acquired information. Each child was assigned a developmental quotient (DQ) in each of the five specific domains. All subjects weretestedbyaprofessionaldoctorintheInstituteofChildHealth Care of Nanjing Maternity and Child Health Care Hospital. Only subjects that had provided finger–prick blood were asked to perform the Gesell test. Finally, 98 of 203 subjects obtained DQs forthefinalanalyses(seetheSM,TableS1).
2.5.Bloodsamplecollectionandleadanalysis
Lead is a known neurotoxicant (ATSDR, 2005). To control for possibleconfoundingfromleadexposure,wetestedthechildren’s finger–prick blood lead levels (Table 1). Blood collection was performed by the Institute of Child Health Care of Nanjing MaternityandChildHealthCareHospitalincompliancewithBlood Lead Clinical Laboratory Technical Specifications released by the MinistryofHealthofChina(MOHC,2006).Leadintotalbloodwas analyzed by graphite furnace atomic absorption spectrometry (GFAAS),whichconsistedofaShimadzuAA–660AASandGFA–4B graphite furnace atomizer (Shimadzu Corporation, Kyoto, Japan). The main parameters used were wavelength 283.3nm, current 8mA, slit width 1.00nm, drying at 150°C, ashing at 325°C, and atomization at 1400°C. The recoveries were 94–102%, with coefficients of variation <20%, from the spikedblood samples.To decreasethepossibilityofcontamination,aspecialistphlebotomist wasappointedandtrained.Theblankcontrolwas4μg/L,andthe limitofquantitationwas10μg/L.Additionalvenousbloodsamples were collected from participants who showed lead levels >100μg/L.
2.6.Statisticalanalysis
PAH concentrations below the detection limit were replaced byhalfofthedetectionlimitvalues.TheKolmogorov–Smirnovtest showed that natural logarithm transformed (ln–transformed) PAH concentrations were normally distributed, as reported previously (Ott, 1990). Thus ln–transformed data were used in the subsequent statistical analysis. The geometric mean (GM) and geometric standard deviation (GSD) were used to describe the distributionofPAHlevels.However,thearithmeticmean,median andrangewerealsousedtocomparethedatawiththatreported in the literature. Pearson’s correlation was used to check for bivariateassociationbetweenln–transformedPAHconcentrations andbehaviorproblemscores,andSpearman'srhocorrelationwas used between PAH concentrations and DQs. Partial correlation tests was performed by controlling blood lead levels among 98 preschool–agedchildren,withPAHs,bloodlead,CBCLsandDQsall tested.Pairedt–testswereusedtoanalyzethedifferencebetween indoorandoutdoordustsamples.TheStudent’st–testwasusedto analyze the difference in PAH concentrations between groups of categorized determinants. DQs were trichotomized using the clinicalcut–offpointaccordingtothenorminChina.Childrenwere thus classified as in the good range (DQш110), normal range (90чDQ<110) or in usual or clinical range (DQ<90). One–way ANOVA was used to check the difference in PAH concentrations between groups of categorized determinants and least significant difference test (LSD) was used for multiple comparisons. Exploratoryfactoranalysiswasconductedonln–transformedPAH concentrations in settled housedust and outdoor dust to identify potentialstructureswithinthedataforexploringthepossiblePAH sources. Factor designations were confirmed using proc factors with method ML and Promax rotation. To explore the possible influencing factors, multiple linear regression analyses were performed with the ln–transformed PAH concentration in indoor
dust as the dependent variable and residence age, floor level, kitchentype,cookingsessionsperday,householdsmokinghabits, frequency of natural ventilation, frequency of vacuuming or cleaning, proximity to a main road and ln–transformed PAH concentrations in outdoor dust as independent variables. All independent variables entered the model backwards and the probability value for inclusion was 0.05 and that for removal was 0.10. p<0.05 was regarded as significant. All analyses were performedusingSPSS16.0(SPSSInc.,Chicago,Illinois).
3.ResultsandDiscussion
3.1.PAHlevelsinsettledhousedustTable 2 presents the summary statistics for PAH concenͲ trationsinsettledhousedust.Eachofthe15PAHsmeasuredwas detected in >90% of dust samples. Total PAH (TPAH) concenͲ trations ranged from 1.2 to 280.4ʅg/g dust, with a GM of 11.1ʅg/g.Phe,FlaandPyrweredetectedin100%ofdustsamples, with GMs of 2.1, 1.8 and 1.4ʅg/g dust, respectively. ConcenͲ trations of low molecular weight (LMW) PAHs with two or three rings ranged from 0.4 to 120.4ʅg/g dust, with a GM of 3.2ʅg/g. For high molecular weight (HMW) PAHs containing four or more rings, concentrations ranged from 0.4 to 160.0ʅg/g dust, with a GMof7.5ʅg/g.
The house–dust PAH concentrations measured in our study were similar to those previously reported for households in the USAin2003(Rudeletal.,2003)andinCanadain2008(Maertens et al., 2008), but much higher than those reported in the USA in 2009(Robertsetal.,2009)and2011(Whiteheadetal.,2011),and in Denmark in 2010 (Langer et al., 2010). A previous report also observed higher PAH floor surface loadings in China compared to theUSAin2008(Naspinskietal.,2008). 3.2.DeterminantsofPAHsinsettledhousedust Inmanycircumstances,suchastheuseofpesticides(Simcox etal.,1995;Nishiokaetal.,2001)andmetalexposure(Charneyet al., 1980; Bonanno et al., 2001), the levels of chemical contaminants on surface soil will represent the material that has been recently deposited on the soil and the fractions of soil that canbemosteasilytransferredindoors.Ofthe15PAHsmeasured in settled house dust, Flu, Phe, Ant, Pyr and BbF showed mild correlationswiththeirlevelsinoutdoordust(0.19чrч0.21,p<0.05). Nap, Ace, Flu, Phe, Fla Pyr and Chr were detected at significantly higher levels in indoor compared with outdoor dust (Table 3). Concentrations of LMW and HMW PAHs and TPAHs were all significantly higher in settled house dust than in outdoor dust (Table 3). These differences should be carefully interpreted becauseofourdifferentdustsamplingmethodsbetweenoutdoor ground and indoor house. Pearson’s correlation test of ln– transformed PAH concentrations in settled house dust revealed that all PAH concentrations were significantly and positively correlatedwitheachother(0.21чrч0.94),exceptforAce(datanot shown).
Factoranalysisshowedtwofactorsforthesettledhousedust data.Thefirstfactor,withloadingш0.5,includedthePAHsPyr,DBA, Chr, BaA, BaP, BkF, BP and IP that had four or more rings. The second factor included Flu, Phe, Ant and Fla, most of which had three rings. Total variances explained by the two factors were 62.6% and 7.7%, respectively (Figure 1a). Two factors were also detected for outdoor settled dust. The first factor, with loading >0.5,includedallPAHsexceptNapandAce,butallthePAHsloaded fortheotherfactorwereall<0.3.Totalvariancesexplainedbythe twofactorswere72.5%and3.7%,respectively(Figure1b).
Table2.MeasurementsofPAHsinsettledhousedust(n=203,unit:ʅg/g)
PAHa RingNo. MDLb(ng/g) >MDL(%) Median Mean GMc±GSDd Range
Nap 2 0.2 97 0.2 0.4 0.2±3.0 nd–6.5 Ace 3 0.2 90 0.4 0.5 0.3±3.0 nd–7.5 Flu 3 0.02 99 0.2 0.3 0.2±2.6 nd–8.7 Phe 3 0.1 100 2.0 3.7 2.1±2.4 0.3–102.6 Ant 3 0.02 95 0.1 0.2 0.1±3.1 nd–2.2 Fla 4 0.4 100 1.8 3.3 1.8±2.7 0.1–72.1 Pyr 4 0.02 100 1.3 2.2 1.4±2.5 0.1–37.7 BaA 4 0.02 98 0.3 0.5 0.3±2.8 nd–3.7 Chr 4 0.04 98 1.4 2.0 1.3±2.6 nd–19.5 BbF 5 0.04 99 0.8 1.1 0.8±2.4 nd–10.3 BkF 5 0.01 98 0.3 0.4 0.3±2.5 nd–2.9 BaP 5 0.02 98 0.4 0.6 0.4±2.7 nd–4.5 DBA 5 0.04 92 0.1 0.2 0.1±3.3 nd–1.6 BP 6 0.02 94 0.4 0.6 0.4±2.6 nd–3.6 IP 6 0.2 92 0.4 0.6 0.4±2.7 nd–4.2 LMW 3.2 5.0 3.2±2.2 0.4–120.4 HMW 7.2 11.3 7.5±2.4 0.4–160.0 TPAH 10.5 16.4 11.1±2.3 1.2–280.4 a Nap:Naphthalene;Ace:Acenaphthene;Flu:Fluorene;Phe:Phenanthrene;Ant:Anthracene;Fla:Fluoranthene;Pyr:Pyrene;BaA:Benz[a]anthracene; Chr:Chrysene;BbF:Benzo[b]fluoranthene;BkF:Benzo[k]fluoranthene;BaP:Benzo[a]pyrene;DBA:Dibenz[a,h]anthracene;BP:Benzo[g,h,i]perylene;IP: Indeno[1,2,3–cd]pyrene;LMW:LowmolecularweightPAHshavingtwoorthreerings;HMW:HighmolecularweightPAHshavingfourormorerings; TPAH:Sumofall15PAHconcentrations; b MDL:Methoddetectionlimit; c GM:Geometricmean; d GSD:Geometricstandarddeviation. Table3.Associationofln–PAHconcentrationsinhousedustsampleswithoutdoordustsamples
PAHa PairedNo. Indoor
(GMb ±GSDc ) Outdoor (GM±GSD) p d re Nap 53 0.3±2.9 0.1±4.0 <0.0001 0.07 Ace 26 0.3±2.3 0.1±3.8 <0.0001 0.10 Flu 62 0.2±2.5 0.1±2.7 <0.0001 0.21f Phe 108 2.5±2.5 1.2±2.7 <0.0001 0.21f Ant 45 0.2±3.1 0.1±2.7 0.10 0.19f Fla 97 2.2±2.7 1.6±2.9 <0.05 0.03 Pyr 108 1.7±2.5 1.2±2.6 <0.001 0.20f BaA 86 0.5±2.6 0.4±3.3 0.34 0.12 Chr 101 1.6±2.7 1.1±3.3 <0.01 0.10 BbF 101 0.9±2.3 0.8±2.8 0.15 0.19f BkF 87 0.4±2.4 0.3±2.6 0.51 0.12 BaP 87 0.5±2.8 0.4±3.6 0.44 0.18 DBA 59 0.1±3.2 0.1±3.0 0.43 0.14 BP 80 0.5±2.7 0.4±3.6 0.31 0.13 IP 84 0.4±2.9 0.4±2.8 0.75 0.11 LMW 110 3.7±2.3 1.5±2.7 <0.0001 0.16 HMW 108 9.1±2.4 6.7±2.8 <0.01 0.12 TPAH 110 13.1±2.3 8.3±2.8 <0.0001 0.13 a Nap:Naphthalene;Ace:Acenaphthene;Flu:Fluorene;Phe:Phenanthrene;Ant:Anthracene;Fla:Fluoranthene;Pyr:Pyrene;BaA:Benz[a]anthracene;Chr: Chrysene; BbF: Benzo[b]fluoranthene; BkF: Benzo[k]fluoranthene; BaP: Benzo[a]pyrene; DBA: Dibenz[a,h]anthracene; BP: Benzo[g,h,i]perylene; IP: Indeno[1,2,3–cd]pyrene;LMW:lowmolecularweightPAHshavingtwoorthreerings;HMW:highmolecularweightPAHshavingfourormorerings;TPAH: sumofall15PAHconcentrations b GM:geometricmean c GSD:geometricstandarddeviation dPairedt–testbetweenindoorandoutdoorln–PAHconcentrations e Pearson’scorrelationcoefficientbetweenindoorandoutdoorln–PAHconcentrations f p<0.05
Chr, BbA, BfA, BkA, BaP, IP, DBA and BP in air declined with increasingfloorlevel(Jungetal.,2011).SimilarresultsforairPAH levelswerefoundintwopreviousstudiesinChina(Lietal.,2005; Taoetal.,2007).
PAH isomeric ratios are useful indicators of PAH sources, because PAH isomers are diluted to a similar extent upon mixing with settled house dust and distribute similarly to other phases because of comparable thermodynamic partitioning and kinetic mass transfer coefficients. The ratio of IP/BP is reported as more reflectiveofcoal/cokeorsmeltingemissions(Dickhutetal.,2000). TheratiosofIP/BPinourstudy(1.17±2.17)areconsiderablyhigher than the 0.33±0.06 observed for automobile emissions, but close to those of coal/coke (1.09±0.03) and smelting (1.03±0.03) (Dickhutetal.,2000).GiventhatcoaliswidelyusedinJiangsufor powergeneration(Pingetal.,2007),coalburningmaybeamore significant source of PAHs in settled house dust in Nanjing comparedwithautomotivesources.
Table4.Linearregressioncoefficients[estimatedɴ(95%confidenceinterval)]associatedwithln–PAHconcentrationsinsettledhousedust
PAHa No. Naturalventilation Floorlevel Residenceage ln–outPAHs R2
Nap 148 0.258(0.013,0.504)b –0.036(–0.068,–0.003)b 0.012(–0.006,0.030) 0.089 Flu 152 0.028(0.005,0.052)b 0.066 Phe 94 – 0.204(0.028,0.381)b 0.054 Ant 78 0.048(0.017,0.078)b 0.113 Fla 153 –0.031(–0.062,0.001) 0.026(0.007,0.044)c 0.090 Pyr 153 0.023(0.006,0.039)c 0.047 BaA 150 –0.037(–0.070,–0.004)b 0.018(–0.002,0.037) Chr 150 –0.253(–0.500,–0.007)b –0.027(–0.058,0.003) 0.056 BbF 151 –0.038(–0.067,–0.009) 0.019(0.002,0.036)b 0.096 BkF 150 –0.199(–0.434,0.036) –0.031(–0.060,–0.001)b 0.022(0.004,0.040)b 0.100 BaP 149 0.032(0.005,0.060)b 0.064 DBA 143 0.031(0.008,0.055)c 0.047 LMW 153 –0.024(–0.048,0.000) 0.018(0.003,0.032)b 0.082 HMW 153 –0.030(–0.058,–0.002)b 0.020(0.004,0.037)b 0.085 TPAH 153 –0.027(–0.052,–0.003)b 0.019(0.004,0.033)b 0.089 a
Nap: Naphthalene; Flu: Fluorene; Phe: Phenanthrene; Ant: Anthracene; Fla: Fluoranthene; Pyr: Pyrene; BaA: Benz[a]anthracene; Chr: Chrysene; BbF: Benzo[b]fluoranthene;BkF:Benzo[k]fluoranthene;BaP:Benzo[a]pyrene;DBA:Dibenz[a,h]anthracene;LMW:lowmolecularweightPAHshavingtwoorthree rings;HMW:highmolecularweightPAHshavingfourormorerings;TPAH:sumof15PAHconcentrations b p<0.05 cp<0.01 Figure2.Associationbetweenln–PAHconcentrationsandthefrequencyofnaturalventilationperday.(a) ln–naphthalene:>4hperdaygroupwas significantlylowerthan1Ͳ4hperdaygroup;(b)lnͲpyrene:>4hperdaygroupwassignificantlyhigherthan<1hperdaygroup;(c)ln–chrysene:>4 hperdaygroupwassignificantlyhigherthan<1hperdaygroup;(d)ln–benzo[k]fluoranthene:>4hperdaygroupwassignificantlyhigherthan<1 hperday.*:p<0.05,one–wayANOVAtestwasusedwithLSDformultiplecomparison;for(b),(c)and(d),PAHconcentrationsamongthreegroups showedlineartrendbyone–wayANOVAtest,p<0.05.
One indoor source of PAHs is thought to be the fumes from cookingoilsusedinthekitchen.TheĮngerprintofoilfumesfrom typical Chinese domestic cooking practices is an abundance of three–ring PAHs (Zhu and Wang, 2003). Our findings of higher levels of three–ring LMW PAHs in settled house dust than in outdoor dust support the theory of cooking oil being the indoor source. However, the outdoor environment appears to be the dominantsourceofPAHsovercookingpractice(62.6%versus7.7% ofvariance).
Like Pyr, Chr and BkF, Nap could also be influenced by the naturalventilationthroughopenwindows.SignificantlylowerNap levelsinhouseswithmorethan4hofnaturalventilationperday werefoundthaninhousesventilatedfor1to4hdaily(Figure2). Multiple linear regression analysis also confirmed that longer natural ventilation led to lower Nap levels [linear regression coefficient and 95% confidence interval, 0.26 (0.01, 0.50)] (Table4). All these results suggest that an indoor source is the mainsourceforNap.
Through 63 pooled observations from urban areas, Maertens etal.(2004)foundthatthePAHcontentofsettledhousedustfrom households with smokers was 3.4–4 times higher than levels in settled dust samples from houses without smokers. However, household smoking was not an important determinant in our analysis, as was reported earlier (Chuang et al., 1995). Only BP showed significantly higher levels in houses where residents smoked(p<0.05,datanotshown).Nosuchdifferenceswerefound for other PAHs. The reason for this may be that although the parents smoked, their smoking might be limited because of the youngageoftheirchildren,orconcernovertheadverseeffectsof smokingontheirchildren.
Pearson’s correlation test showed that all PAHs were significantlyandpositivelyassociatedwithresidenceage,withthe
rvaluerangingfrom0.172to0.301,exceptforAce,Chr,BPandIP.
Multiplelinearregressionanalysisshowedthatresidenceagewas associated with most PAHs, and older dwellings were associated with higher PAH concentrations (Table 4). A recent study in Northern California reported that residence age had the most significant effect on total house–dust PAH concentrations, with olderhouseshavinghigherPAHconcentrations(Whiteheadetal., 2011). The same effects were found for house–dust nicotine concentrations in an earlier study (Whiteheadet al., 2009). Given that almost 95% of the total dust loading present in a carpet residesdeepwithinthecarpetandwillnotberemovedbytypical cleaning (Roberts et al., 2004), it was concluded that environͲ mental contaminants can accumulate in household carpets over yearsordecades(Robertsetal.,2009).Inourstudy,however,only about 5% of houses were carpeted with a small rug in the living room. Nevertheless, we found a significant association between residenceageandhouse–dustPAHlevels.Thismightbeexplained by the fact that in many places, such as beneath beds or behind furniture, house dust could remain for a long time. Alternatively, PAHs could act like certain pesticides, which adhere to building materialsandarereleasedovertime(Clarketal.,2002).However, thisneedsfurtherinvestigation. Otherdeterminantsthathavebeenlinkedtohouse–dustPAH levelsinpreviousstudies,suchasfrequencyofcleaning(Maertens etal.,2008)andtrafficemissionsortrafficdensity(Whiteheadet al., 2011), were not deemed important determinants in our analysis. In terms of the influence of vehicular traffic, we used a dichotomousvariableof“<500metersfromthechild’shometoa two– or more–lane motorway”, which might be too crude to establish a possible association. We also failed to establish any influenceofcookingpractices.Separatekitchensandlessfrequent
cooking did not appear to reduce PAH levels in house dust. One possible reason for this might be that occupants in houses with open kitchens were inclined to select a better quality ventilation hoodcomparedtothosewithseparatekitchens.
3.3.HealthriskofPAHsinsettledhousedust
Behaviorproblemscoresanddevelopmentalquotientsofthe preschool–aged children were used to assess the risks of PAHs in settled house dust. Pearson’s correlation coefficients (Table 5) showed that most PAHs were positively associated with internalizingproblemscores,ofwhichBaPandIcdPwerepositively associatedwithmostbehavioralproblemscores.Inclusionofblood lead as a covariate did not materially alter this significant associationin98preschool–agedchildren(datanotshown).These results suggested that higher PAHs might cause more behavior problems. Although Spearman’s rho correlation test showed no significant association between PAH levels and Gesell DQs (data notshown),higherBaPandBPshowedlowerGeselllanguageDQs, and higher Chr and BkF were associated with lower Gesell social skillDQsaftertheDQsweretrichotomizedintogood,normaland usualorclinicalrange(Figure3).Theseresultsshouldbecarefully interpreted because the correlation coefficient between BaP and BPwas0.84andwas0.89betweenChrandBkF.Inthisanalysis,an obvious association between LMW PAHs and health risk was not observed.Thismaybeexplainedbytheirtemperature–dependent gas–particle partitioning behavior. The concentrations of LMW PAHs, like naphthalene and acenaphthene, in settled house dust mightnotrepresenttheirtotalbodyexposureamountsbecauseof theirpreferentialpresenceinthevaporphase(Gevaoetal.,2007).
Laboratory studies exposing experimental animals to PAHs during the prenatal and neonatal periods have reported impairmentsofmemoryandlearning(Wormleyetal.,2004;Brown et al., 2007), as well as anxiety and depression behavior effects (Saundersetal.,2002;Saundersetal.,2003;Saundersetal.,2006). SeveralcohortstudiesintheUSA(Pereraetal.,2006;Pereraetal., 2011;Pereraetal.,2012a),China(Tangetal.,2008;Pereraetal., 2012b) and Poland (Edwards et al., 2010) have reported neurodevelopmental effects of PAHs in humans. All found evidence that prenatal exposure to PAHs may have an adverse effectontheneurodevelopmentofchildrenaged3–8years.Tothe best of our knowledge, our results are the first to report the possibleassociationofpostnatalsettled–dustPAHsexposurewith behavior and neurodevelopmental problems in preschool–aged children.However,thelowparticipationratemayhaveintroduced abias.However,wecheckedtheCBCLbehaviorproblemscoresof thoseparticipantswithoutDQs,andnodifferencewasfoundfrom thosewithDQs.Thesmallsamplesizemeantthatourstudycould not include multivariate statistical analysis, which may decrease thestatisticalpowerofouranalysesandindicatedthatfollowupin largerstudiesisrequired.
SettleddustPAHexposurelevelsweremeasuredatthesame timeastheneurodevelopmentoutcomesandthismaycomplicate the interpretation of any association. Whitehead et al. (2012) reported that variance ratios for PAHs in residential dust are generallymodestwhenrepeatdustsamplesarecollectedatsemi– annual intervals. They further tested the long–term variability in repeated residential – dust samples collected at intervals of 3– 8years. Their findings indicated that it may be feasible to use residentialdustfor retrospective assessment of PAH exposures in studiesofhealtheffects,especiallyifdustsamplescanbecollected within 5 years of the relevant exposure (Whitehead et al., 2013). Thus,ourdustmeasurementsmaybesufficienttocharacterizethe average levels of PAHs found in the dwellings of preschool–aged childrenovertheyearsafterbirth.
Table5.Associationbetweenln–PAHconcentrationsanddifferentneurobehaviorscores.PresentedvaluesarePearsoncorrelationcoefficients(n=203)
PAHa
Somatic Anxious Withdrawn Social Thought Attention Compulsive Aggressive Internalizing Externalizing Total problems Nap 0.083 0.136 0.092 0.121 0.144 0.052 0.236 0.154 0.213b 0.130 0.181 Ace 0.125 0.071 0.066 0.193 0.087 0.094 0.406b 0.185 0.176 0.154 0.168 Flu 0.155 0.115 0.071 –0.058 0.046 –0.052 0.282 0.151 0.144 0.105 0.127 Phe 0.114 0.162 0.044 –0.015 0.046 –0.117 0.247 0.132 0.168 0.067 0.124 Ant 0.067 0.185 0.049 0.015 0.086 –0.086 0.327 0.140 0.177 0.086 0.135 Fla 0.088 0.189 –0.013 0.067 0.047 –0.168 0.266 0.100 0.178 0.021 0.101 Pyr 0.158 0.165 0.046 0.095 0.104 –0.072 0.336 0.150 0.207b 0.096 0.161 BaA 0.112 0.167 0.063 0.218 0.106 –0.049 0.325 0.122 0.204b 0.090 0.154 Chr 0.115 0.176 0.016 0.199 0.071 –0.105 0.37 0.092 0.200b 0.043 0.126 BbF 0.155 0.157 0.087 0.133 0.125 –0.079 0.428b 0.122 0.219b 0.089 0.162 BkF 0.126 0.182 0.070 0.076 0.133 –0.060 0.379 0.126 0.221b 0.086 0.163 BaP 0.182 0.268c 0.149 0.150 0.164 0.085 0.509c 0.242b 0.313c 0.214b 0.276c DBA 0.146 0.109 0.085 –0.044 0.129 0.054 0.413b 0.106 0.188 0.092 0.151 BP 0.167 0.016 –0.014 0.180 0.110 –0.053 0.366 0.04 0.128 0.003 0.065 IP 0.211b 0.264c 0.163 0.035 0.165 0.113 0.463b 0.248b 0.310c 0.242b 0.296c LMW 0.103 0.148 0.045 0.001 0.043 –0.106 0.272 0.144 0.163 0.082 0.127 HMW 0.151 0.179 0.066 0.117 0.097 –0.072 0.336 0.141 0.223b 0.090 0.166 TPAH 0.138 0.172 0.056 0.080 0.080 –0.084 0.329 0.143 0.208b 0.088 0.157 a Nap:Naphthalene;Ace:Acenaphthene;Flu:Fluorene;Phe:Phenanthrene;Ant:Anthracene;Fla:Fluoranthene;Pyr:Pyrene;BaA:Benz[a]anthracene;Chr: Chrysene; BbF: Benzo[b]fluoranthene; BkF: Benzo[k]fluoranthene; BaP: Benzo[a]pyrene; DBA: Dibenz[a,h]anthracene; BP: Benzo[g,h,i]perylene; IP: Indeno[1,2,3–cd]pyrene;LMW:lowmolecularweightPAHshavingtwoorthreerings;HMW:highmolecularweightPAHshavingfourormorerings;TPAH: sumofall15PAHconcentrations b p<0.05level(2–tailed) c p<0.01level Figure3.Associationbetweenln–PAHconcentrationsandDQscores.(a) ln–benzo[a]pyreneandlanguageDQs:lineartrendtest, p=0.014;LSDtest,p<0.05for<90groupcomparedto>110group;(b)ln–benzo[g,h,i]peryleneandlanguageDQs:lineartrendtest, p=0.054;(c)ln–chryseneandsocialskillDQs:lineartrendtest,p=0.030;LSDtest,p<0.05for90–110groupcomparedto>110group; (d)ln–benzo[k]fluorantheneandsocialskillDQs:lineartrendtest,p=0.049.
Collecting only one dust sample from the area where a child playsregularlyinahomewouldreducethestatisticalpowerofan analysis. However, our sampling was not restricted to one room, buttypicallyincludedalltheplaceswhereachildplayedfrequently intheirhome.Otherstudieshavetestedtheusefulnessoftheone– sample approach and household vacuum cleaners to evaluate the contentofhousedustinepidemiologicalstudies(Coltetal.,2008; Whitehead et al., 2009; Whitehead et al., 2011). Simultaneously, we measured the profiles of a wide range of PAHs to assess the cumulative neurodevelopmental risks from exposure to PAHs. Single urinary biomarker of PAHs, like hydroxy–Pyr, may not be sufficientforassessingcumulativeexposuresandrisks,althoughit hasbeenwidelyusedtoassessenvironmentalPAHexposurelevels (Viauetal.,2002;Zhuetal.,2009).Forinstance,Fluwasreported tobenegativelyassociatedwiththyroidhormonelevels(Zhuetal., 2009),andNapwasreportedtobeassociatedwithsmokinghistory (Nethery et al., 2012). Our results also suggested that high molecularweightPAHs,likeBaP,IcdPandBghiP,whichareexcreted primarily in the feces (Li et al., 2008), showed more association with neurodevelopmental abnormality. Thus, to measure the profilesofawiderangeofPAHsinsettleddustinsteadofasingle urinary biomarker is preferred for the assessment of exposure to high molecular weight PAHs and associated neurodevelopmental risks.
4.Conclusions
In summary, the 15 tested PAHs are ubiquitous in urban settledhousedustandmaybeinadvertentlyingestedbychildren living in Nanjing, China. Coal burning in the outdoor environment andcookingoilfumesareprobablythetwomainsourcesofindoor PAHs. Natural ventilation, floor level and residence age can potentially influence house–dust PAH levels. Our findings of a potential adverse effect of postnatal exposure to PAHs on the behavior and neurodevelopment of preschool–aged children require follow up in larger studies. This study highlights the importance of assessing the effects of settled–house dust PAH exposurepostnatallyduringtheearlyyearsoflife.
Acknowledgements
Wearegratefultothefamiliesfortheirparticipationthehome inspectors who assisted with the collection of the dust samples, and the undergraduate students: Mao Liu, Yuan Cun, Xue Yang, Yue–Jiao Chen and Shan–Shan Chen, who helped the home inspectors to collect the house dust samples and occupant information. This study was partly supported by grants from the National Natural Science Foundation of China (Nos. 81072268, 81372955), the Natural Science Foundation of Jiangsu Province of China (No. BK2010535), Jiangsu Postdoctoral Research Funds (1001017C), and the Priority Academic Program Development of JiangsuHigherEducationInstitutions.
SupportingMaterialAvailable
Information on Dust Collection, Neurodevelopmental tests of thesubjects(TableS1).Thisinformationisavailablefreeofcharge viatheInternetat:http://www.atmospolres.com.
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