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Air Pollution and Retained Particles in the Lung Brauer, Michael; Avila-Casado, Carmen; Fortoul, Teresa I.; Vedal, Sverre; Stevens, Bonnie; Churg, Andrew Oct 31, 2001

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Environmental Health Perspectives • VOLUME 109 | NUMBER 10 | October 2001 1039Air Pollution and Retained Particles in the LungMichael Brauer,1,2 Carmen Avila-Casado,3 Teresa I. Fortoul,4 Sverre Vedal,2 Bonnie Stevens,5 and Andrew Churg51School of Occupational and Environmental Hygiene, and 2Department of Medicine, The University of British Columbia, Vancouver,British Columbia, Canada; 3Instituto Nacional de Cardiologia Ignacio Chavez, Mexico City, Mexico; 4Departament of Cellular and TissueBiology, Faculty of Medicine, Universidad Autonoma de Mexico, Mexico City, Mexico; 5Department of Pathology, University of BritishColumbia, Vancouver, British Columbia, Canada Epidemiologic studies indicate that currentlevels of particulate air pollution are associatedwith adverse health outcomes, includingincreased cardiopulmonary mortality (1,2).Although evidence suggests that short-termimpacts of particulate air pollution are dis-placing deaths by more than months, ofgreater public health significance is the poten-tial for long-term impacts that may shortenlives by years or that may lead to chronic car-diopulmonary morbidity. Several prospectivecohort studies provide evidence of such long-term effects, including associations betweenambient particles and lung cancer (3–5).Whereas acute effects may be limited to thoseindividuals with existing cardiopulmonarydisease, chronic exposures may affect a muchlarger proportion of the exposed population.Although the epidemiologic evidence pointsto a causal relationship with particles originat-ing in combustion processes, the biologicalmechanism(s) as well as the exact types andsizes of particles involved are the subjects ofintensive investigation. One hypothesis is thatthe ultrafine particle size fraction is responsi-ble for the epidemiologic observations (6).This hypothesis is partly based on the factthat the majority of atmospheric particles, bynumber, are in the ultrafine mode. These par-ticles, produced in combustion processes, arelikely to contain condensates of toxic metalsand surface acidity. In animal models, ultra-fine particles appear to induce an intenseinflammatory reaction and are believed to betranslocated to the pulmonary interstitium inlarge numbers (7,8). Despite the interest in the topic, little isknown of the types, sizes, and locations ofambient atmospheric particles in humanlungs. Direct measurements of deposited par-ticles in humans are difficult, but animalmodels show that virtually all types of inhaledparticles can be translocated across the alveo-lar epithelium to the interstitium, from whichlocation they are cleared slowly or not at all(9). Analysis of lung parenchymal particleburden can thus provide an indication of thetypes and numbers of particles to which anindividual has been exposed. Also, such analy-ses can show where potentially toxic particlesaccumulate. Recently, we used analytical elec-tron microscopy to determine parenchymalparticle burden in the lungs of long-term resi-dents of Vancouver who had never smokedtobacco (10). Our analysis indicated that96% of the retained particles were < 2.5 µmin aerodynamic diameter (PM2.5), thereforesuggesting that epidemiologic investigationsshould focus on this size class of particles. In demonstrating biological plausibility itis important to establish a link betweenambient concentrations, exposure, and dose.In this study we examined lungs from female,nonsmoking, long-term residents of MexicoCity, Mexico, a region with high ambientparticle levels, and Vancouver, BritishColumbia, Canada, a region of much lowerlevels. In doing so we asked a fundamentalquestion: Does residence in a location withhigh air pollution levels result in a higherlevel of biologically delivered dose of pollu-tants? It is our hypothesis that exposure tohigh levels of particulate air pollution isreflected in increased interstitial particle bur-dens. Although this hypothesis may appearsimplistic, there has been no direct demon-stration that increased ambient particle expo-sure in fact results in higher particle retention(and, by implication, deposition) in the lungover a lifetime. Such a finding would providepathologic evidence to support the epidemio-logic data associating particulate matter expo-sure with adverse health outcomes such asmortality. This would provide additional evi-dence that the observed epidemiologic associ-ations, especially those related to chronicexposures, are in fact biologically plausible. Afailure to prove this hypothesis would suggesteither that the observed epidemiologic associ-ations may be driven by soluble particles(which would be cleared from the airwaysand parenchyma) or that the epidemiologicfindings are not valid and hence argue againsttheir plausibility.Materials and MethodsCase selection. The study protocol wasreviewed and approved by the University ofBritish Columbia Clinical Research EthicsBoard (Approval C96-0511). Lungs for thisstudy were obtained from a general autopsyservice at a cardiovascular referral hospital inMexico City and were compared to lungsobtained from a general hospital autopsy pop-ulation in Vancouver. To reduce the possibil-ity of occupational dust exposures, only lungsfrom women were examined. Occupational,smoking, and residential histories wereAddress correspondence to M. Brauer, School ofOccupational and Environmental Hygiene,University of British Columbia, 2206 East Mall,Vancouver, BC, V6T 1Z3 Canada. Telephone:(604) 822-9585. Fax: (604) 822-9588 E-mail:brauer@interchange.ubc.caThis work was supported by grants from theBritish Columbia Lung Association and theMedical Research Council of Canada. M. Braueracknowledges the support of a Career InvestigatorAward from the American Lung Association and aScientist Award from the Medical ResearchCouncil of Canada and the British Columbia LungAssociation. Received 17 January 2001; accepted 4 April 2001.ArticlesEpidemiologic evidence associates particulate air pollution with cardiopulmonary morbidity andmortality. The biological mechanisms underlying these associations and the relationship betweenambient levels and retained particles in the lung remain uncertain. We examined the parenchymalparticle content of 11 autopsy lungs from never-smoking female residents of Mexico City, aregion with high ambient particle levels [3-year mean PM10 (particulate matter ≤ 10 µm in aero-dynamic diameter)= 66 µg/m3], and 11 control residents of Vancouver, British Columbia,Canada, a region with relatively low levels (3-year mean PM10 = 14 µg/m3). Autopsy lungs weredissolved in bleach and particles were identified and counted by analytical electron microscopy.Total particle concentrations in the Mexico City lungs were significantly higher [geometric mean= 2,055 (geometric SD = 3.9) × 106 particles/g dry lung vs. 279 (1.8) × 106 particles/g dry lung]than in lungs from Vancouver residents. Lungs from Mexico City contained numerous chain-aggregated masses of ultrafine carbonaceous spheres, some of which contained sulfur, and aggre-gates of ultrafine aluminum silicate. These aggregates made up an average of 25% of the totalparticles by count in the lungs from Mexico City, but were only rarely seen in lungs fromVancouver. These observations indicate for the first time that residence in a region with high lev-els of ambient particles results in pulmonary retention of large quantities of fine and ultrafine par-ticle aggregates, some of which appear to be combustion products. Key words: air pollution,environmental exposure, particles, pulmonary retention. Environ Health Perspect 109:1039–1043(2001). [Online 27 September 2001]http://ehpnet1.niehs.nih.gov/docs/2001/109p1039-1043brauer/abstract.htmlobtained by interviews with relatives using astandardized questionnaire. All subjects werelifetime nonsmokers, and none had knownoccupational dust exposure, including, forthe Mexico City lungs, domestic woodsmoke exposure. Exposure to environmentaltobacco smoke was assessed by evaluation ofcalcium particles in tissue samples. Retainedcalcium particles indicate exposure totobacco smoke (11). The lungs from Mexicowere collected from women who had beenlifetime residents of Mexico City, and thelungs from Vancouver were from residentswho had lived in Vancouver for ≥ 20 years.In both locations, inclusion criteria wererestricted to cases > 60 years old at time ofdeath. The mean ages were 67 ± 19 (SD) and64 ± 9 years for Vancouver and Mexico City,respectively. None of the patients had died oflung disease, and the lungs were all morpho-logically normal except for the presence ofminor degrees of pneumonia at autopsy.Four additional cases from Mexico City wereexamined, but three were excluded becauseparticle levels in the samples were too high toallow for quantitative electron microscopyanalysis. An additional sample from MexicoCity was excluded because approximately30% of the particles were determined to con-tain calcium, an indicator for tobacco smokeexposure (11). The total number of retainedparticles for this case was similar to the othercases from Mexico City. Four additional casesfrom Vancouver were analyzed, but wereexcluded from the data analysis because inter-views could not be conducted; consequentlyoccupational histories were not obtained. Forthree of these cases, retained particle concen-trations were similar to the other cases fromVancouver, whereas the concentrations fromthe fourth case, which appeared to be an out-lier, were significantly higher.Tissue dissection and particle countingprocedure. All tissues were handled withdust-free gloves. Dissections were performedon formalin-fixed lungs using a dissectingmicroscope. From each specimen, we selectedfor analysis a sample of parenchyma weighing1–2 g from the central portion of the lung,avoiding large airways, and an equivalent sizesample that was dried to constant weight toallow expression of results as particles pergram dried tissue. We selected the central tis-sue sample so that we would analyze compa-rable tissues from Vancouver and MexicoCity cases. Tissue samples were dissolved inbleach and centrifuged at 30,000 × g for 20min; the sediment was washed once toremove the bleach and recentrifuged at30,000 × g for 20 min to ensure that verysmall particles were not lost during prepara-tion. The preparation was resuspended andcollected on 0.1µm filters (Millipore-MF;Millipore Corp., Bedford, MA, USA) andthen transferred to coated electron micro-scope grids (10). We previously showed thatthis approach effectively collects particles of≥ 0.010 µm (12).For this study, particles larger than0.010 µm were counted, sized, and identi-fied using an electron microscope (Phillips400T; Phillips Electronics, Alomelo, TheNetherlands) equipped with an energy dis-persive X-ray spectrometer (Kevex; Thermo-Kevex X-Ray, Scotts Valley, CA, USA).Approximately 100 particles were countedper sample; particles were measured andidentified by a combination of morphologyand chemistry as determined by X-ray spec-troscopy. For this study particles were charac-terized as silica, silicates, singlet particles ofmetals (particles analyzing only as iron,Articles • Brauer et al.1040 VOLUME 109 | NUMBER 10 | October 2001 • Environmental Health PerspectivesTable 1. Concentrations of particles (millions of particles per gram of dry tissue) of different types countedin individual samples of lungs from Vancouver residents.Metals Carbon +(single Carbon sulfur Kaolin-like IronSample Silica Silicate particles) Agg Agg Agg Agg Misc42318 67 280 75 ND ND ND ND 842313 9 40 16 ND ND ND ND ND42324 81 119 46 ND ND ND ND ND42304 60 143 56 ND ND ND ND ND42329 145 220 95 ND ND ND ND ND2458 307 119 72 ND ND ND ND ND2459 249 49 16 ND ND ND ND ND2460 325 150 40 ND ND ND ND ND2461 56 71 62 ND 2 ND ND ND2464 105 139 84 ND ND ND ND ND2467 66 88 35 ND ND ND ND NDMean 133 128 54 0 0.2 0 0 0.7SD 109 7 26 0 0.6 0 0 2.4Percent of totala 37.9 43.0 18.8 0.0 1.0 0.0 0.0 1.9Abbreviations: Carbon Agg, aggregated particles producing no X-ray peak; Carbon + Sulfur Agg, aggregrated particlesproducing only a sulfur X-ray peak; Iron Agg, aggregated particles analyzing as iron, sometimes with a small silicon peak;Kaolin-like Agg, aggregated particles with a composition similar to kaolinite; Misc, miscellaneous; ND, not detected. aMean percentage of each type of particle relative to the total number of all types of particles for each case. Table 2. Concentrations of particles (millions of particles/g dry tissue) of different types counted in indi-vidual samples of lungs from Mexico City residents. Metals Carbon +(single Carbon sulfur Kaolin-like IronSample Silica Silicate particles) Agg Agg Agg Agg Misc2416 128 132 48 48 ND 135 10 162417 252 1,619 352 100 100 353 ND ND2418 217 1,026 116 ND 16 150 251 172419 366 230 107 53 32 97 ND 532420 192 187 42 16 16 11 37 ND2423 316 185 86 95 23 24 ND 232425 7,262 11,923 2,604 3,776 ND 871 ND ND2426 173 236 79 165 52 43 ND 252427 770 1,057 258 542 171 199 ND ND2428 3,395 8,068 4,243 3,820 1,697 848 ND 2122448 319 1,033 73 344 25 442 ND 24Mean 1,217 3,915 1,384 1,537 549 312 132 71SD 2,215 2,336 728 895 236 288 99 52Percent of total 24.6 38.2 10.1 10.9 3.2 9.3 2.1 1.6Abbreviations: Agg, aggregated particles; Misc, miscellaneous; ND, not detected.aMean percentage of each type of particle relative to the total number of all types of particles for each case.Figure 1. (Ln)Concentration of total particles pergram of dry tissue in Mexico City and Vancouversamples. The top and bottom of boxes indicate the25th and 75th percentiles, respectively, and thelength of boxes is interquartile distance. Upperand lower whiskers extend to the largest andsmallest measured values that are 1 interquartiledistance from the 75th and 25th percentiles,respectively. Circles are data points that aregreater or less than 1 interquartile distance fromthe 75th or 25th percentiles. The line inside the boxindicates the median value. 252423222120191817In (no. of particles/g dry tissue)Mexico City(n = 11)Vancouver(n = 11)Locationaluminum, or titanium), and aggregated par-ticles (Tables 1 and 2). With one exception,the aggregated particles were only seen inMexico City lungs. We classified aggregatedparticles as follows: a) purely carbonaceous ifthey were composed of more or less sphericalparticles that produced no X-ray signal [wepreviously demonstrated our ability to detectpurely carbonaceous aggregates by carrying asample of pure ultrafine carbon black throughour preparative procedure, including adding asample to lung tissue (12)]; b) carbonaceous +sulfur if they had a similar morphologicappearance but produced a small sulfur peak;c) kaolinite-like if they were composed ofplaty particles with an aluminum:silicon ratiosimilar to kaolin; and d) iron aggregates ifthey produced X-ray peaks for iron or ironwith a small amount of silicon. For purposesof calculating particle numbers and sizes, wetreated each aggregate as one particle, but wemade additional measurements to determinethe sizes of particles that made up the car-bonaceous and carbon + sulfur aggregates.Retained particle concentrations were notnormally distributed and were therefore log-transformed before all statistical analyses.Ambient air samples. A limited numberof ambient PM2.5 particle samples were col-lected on filters in Mexico City andVancouver. The purpose of this samplingwas to establish whether the types of parti-cles observed in tissue samples were of simi-lar composition and morphology to thosefound in ambient air. All particle sampleswere collected by intermittent sampling (1min of sampling in each 8-min period, for atotal of 1,440 min) over a 7-day period inorder to provide a sample that was represen-tative of typical particle types. In both loca-tions, samples were collected betweenOctober 1999 and January 2000. Particleswere collected with Harvard Impactors onpolytetrafluoroethylene (Teflon) membrane(Teflo; Pall Life Sciences, Ann Arbor, MI,USA) filters at a flow rate of 4 L/min. InVancouver, samples were collected at aNational Air Pollution Surveillancemonitoring site (Kitsilano), and in MexicoCity, samples were collected at two sites thatare part of the Mexico City ambient moni-toring network: one located in the center ofthe city (Hangares) and another in thesouthwest (Tlalpan). Three-year averagePM10 concentrations were 66 µg/m3 forseven monitoring sites in Mexico City and14 µg/m3 from nine sites in Vancouver (13). After sample collection, filters wereweighed and then processed for electronmicroscopy. The filters were wet with 0.1mL of 95% ethanol, sonicated in 1 mL of dis-tilled, deionized water, centrifuged, and trans-ferred to electron microscope grids followingthe same procedures used for the tissue samples.ResultsWe found significantly higher (p < 0.001, t-test) concentrations of retained particles intissue samples from Mexico City than inthose from Vancouver (Figure 1, Tables 1and 2). The geometric mean total particleconcentrations in the Mexico City lungs was2,055 × 106 particles/g dry lung [geometricSD (GSD) = 3.9] as compared to 279 (GSD= 1.8) × 106 particles/g dry lung in theVancouver samples, a nearly 10-fold differ-ence. Examination of individual mineralspecies showed higher particle concentra-tions in the Mexico City samples for everyparticle type examined (compare mean con-centrations in Tables 1 and 2).In addition to the mixture of silicatesand other crustal material typically found intissue samples, the samples from MexicoCity contained on average 25.5% aggregatedultrafine particles (Table 2). In particular, weobserved chain aggregates of approximatelyspherical particles that produced no energydispersive X-ray signal and were, therefore,presumably carbonaceous (Figure 2). Manyof these also contained trace amounts of sul-fur, which is suggestive of combustionsource particles. The morphology of thechain aggregates was remarkably similar tothose isolated from Mexico City ambient airsamples (Figure 2A) and from diesel exhaust(14). In sharp contrast to the Mexico Citysamples, only 1 aggregate (carbonaceous +sulfur) was detected in the 11 Vancouver tis-sue samples (Table 1). In Mexico City tissuesamples, a large number of aluminum sili-cate aggregates with a chemical compositionsimilar to kaolinite were also identified, aswere occasional aggregates consisting of ironparticles that also gave a small X-ray peak forsilicon. The origin of these particles wasunclear, but they were never observed inVancouver lungs. On average, the aggregatedcarbonaceous particles and carbonaceous par-ticles + sulfur made up 14% of the total par-ticles; the kaolinite-like aggregates made up9%, and the iron aggregates 2% (Table 2).However, if every particle in the aggregateswas counted as a single particle, these parti-cles would make up the vast majority of theparticles detected in the Mexico City tissuesamples. Tables 3 and 4 show the sizes of particlesin the lung tissue samples from the two sites.Overall, the geometric mean particle size inthe lungs was similar in both cities, with amean for all of the cases of 0.35 µm forMexico City samples and 0.39 µm forVancouver samples. Table 4 also shows thegeometric mean diameters for the aggregatedparticles detected in lungs from MexicoCity. Some of the aggregates were quitelarge, ranging up to about 4 µm, but mostwere smaller than 1 µm. Table 5 shows themean sizes of the particles that made up thecarbonaceous and carbon + sulfur aggregates.These were almost all ultrafine particles. Thestructure of the kaolinite-like aggregates andiron aggregates prevented measurement ofindividual particle sizes.Comparison of air samples from the twolocations indicated a similar distinction inoverall mass (and particle number) concen-trations and in composition, with more than20 times as many aggregates observed inArticles • Air pollution and retained particlesEnvironmental Health Perspectives • VOLUME 109 | NUMBER 10 | October 2001 1041Figure 2. Representative illustration of chained aggregated spherical particles giving no signal (i.e., car-bonaceous particles) from (A) a Mexico City air sample and (B) a Mexico City lung. Bars = 0.1 µm.Table 3. Geometric mean (GSD) particle diame-ters (µm) for individual samples of lungs fromVancouver.Carbon + Sample All particles sulfur Agg42318 0.69 (2.3) ND42313 0.69 (2.2) ND42324 0.52 (2.2) ND42329 0.65 (2.5) ND2458 0.31 (2.7) ND2459 0.22 (2.3) ND2460 0.33 (2.4) ND2461 0.31 (2.6) 0.33 (0)a2464 0.31 (2.3) ND2467 0.34 (2.3) NDND, not detected. Each aggregate was counted as oneparticle. No carbon aggregates, kaolin-like aggregates,or iron aggregates were detected in any of the samplesfrom Vancouver.aOnly one aggregate identified. Mexico City samples than in those collectedin Vancouver. A more quantitative compari-son was not possible because many of theambient samples collected in Mexico Citycontained too many aggregates to reliablycount. For the limited samples that we col-lected, the mean PM2.5 particle mass concen-tration measured in Mexico City was 29.5µg/m3 (n = 11) compared to a mean concen-tration of 10.5 µg/m3 for the samples (n = 6)collected in Vancouver. The geometric meandiameter of ambient carbon aggregates(counting the entire aggregate as one particle)from Mexico City was approximately 1.1µm, with individual particles within theaggregates in the range of 0.04– 0.15 µm.Because of their complex morphology, it wasnot possible to determine individual particlesizes for the kaolinite-like aggregates observedin air samples collected in Mexico City. Discussion Our observations indicate that long-termresidence in an area of high ambient particleconcentrations is associated with greaternumbers of retained particles in the lung;this shows for the first time that the aggre-gated ultrafine particles in ambient air canalso be found in lung tissue. Our ability todetect retained aggregated ultrafine particlesprovides evidence that aggregates in air donot disaggregate once they are inhaled,although the sizes in tissue samples wereslightly smaller than in air. We cannot deter-mine absolutely if the aggregates weobserved in tissue samples are the same asthose observed in air samples. However, thesimilarities between the two (Figure 2) makeit unlikely that the aggregates observed inthe lungs form after inhalation of airborneultrafine particles or that they are artifacts ofthe extraction procedure.This work, and conclusions that may bedrawn from it, is subject to several limitations.In both locations, we observed a large degreeof intersubject variability in numbers ofretained particles (Figure 1, Tables 1 and 2).This is likely the result of variable exposures aswell as interindividual differences in particleclearance and translocation efficiency.Although we have clearly found a differencein the number of retained particles betweentissue samples of residents of Vancouver andMexico City, we were unable to identify dif-ferences in the numbers of retained particlesin individuals living in higher and lower pol-lution regions of Mexico City. Because of the complexity of the analysisand the difficulties in obtaining autopsy sam-ples that meet our inclusion criteria (non-smoking women > 60 years at death, > 20year residence in Vancouver or Mexico City,no occupational dust exposure, no deathsfrom respiratory disease), our sample size waslimited and the measured concentrations ofretained particles should not be consideredquantitatively representative of those for indi-viduals living in Vancouver or Mexico City.However, our analysis shows that the samplesize was sufficient to indicate a statisticallysignificant difference between the groupsfrom the two locations. The exclusion of foursamples from Mexico City with particle levelsthat were too high to allow for quantitativeelectron microscopy analysis does not alterthis finding. Had we been able to quantifythe high particle levels on these samples, thedifferences between the two locations wouldhave been even greater. Our inclusion criteria allowed us to atleast partially control for confounding by sex,smoking, age, and duration of residencewhile we also screened samples for calciumparticles as indicators of environmentaltobacco smoke exposure. Although webelieve that these are the major potential con-founding variables of concern for this analy-sis, it is possible that other unrecognizedfactors pertaining to differences between thestudy populations from the two locationscontributed to the observed differences. The number of retained particles weobserved is certainly a marked underestimateof the number inhaled because many particlesare soluble and therefore would not bedetected by our procedures. Further, our ana-lytical approach cannot differentiate betweenparticles originating in airspaces and thosethat have entered the interstitium, so that wecannot determine what proportion of mea-sured particles have been very recentlyinhaled. However, our data clearly indicatethat, despite exposure to similar types of parti-cles, individuals who reside in an area of highcompared to low ambient particle concentra-tions retain much greater numbers of ambientparticles. This finding may seem trivial, but itshould be considered in the context of the lowmass concentrations of particles in ambientair compared to occupational dust exposuresthat lead to disease. This finding suggests thateven the gravimetrically small particle burdenfound in regions with high concentrations ofambient particles is able to overwhelm localclearance mechanisms, presumably as a resultof particle toxicity.In conclusion, we observed significantlyhigher numbers of retained particles in lungtissue samples from long-term residents ofMexico City, a region with high ambient airpollution, relative to samples from long-termresidents of Vancouver, a region with muchlower ambient pollution levels. Because werestricted our analysis to tissue samples fromnonsmoking women, it is likely that the dif-ferences observed were due to differences inambient exposures. Additionally, aggregatesof ultrafine particles can be found in largenumbers in the lungs of individuals fromMexico City, but were only rarely observed insamples from Vancouver. These particles aremorphologically and chemically similar toparticles found in ambient air, and at leastsome of these particles appear to be combus-tion derived on the basis of morphologic andchemical similarities to particles from motorvehicle exhaust. Our observations demon-strate, therefore, that long-term exposure toambient particles, and especially to aggregatedambient ultrafine combustion products,results in higher retention of these particles inlung tissue. Because the findings demonstrateArticles • Brauer et al.1042 VOLUME 109 | NUMBER 10 | October 2001 • Environmental Health PerspectivesTable 4. Geometric mean (GSD) particle diameters (µm) for individual samples of lungs from Mexico City.All Carbon Carbon +Sample particles Agg sulfur Agg Kaolin-like Agg Iron2416 0.47 (2.6) 0.40 (2.0) ND 0.65 (2.3) 0.13 (1.2)2417 0.39 (2.5) 0.56 (2.1) 0.48 (1.1) 0.52 (1.3) ND2418 0.23 (2.5) ND 0.89 (1.1) 0.78 (2.1) 0.62 (1.7)2419 0.41 (2.4) 0.44 (1.7) 2.0 (2.8) 0.61 (1.5) ND2420 0.37 (2.5) 0.32 (1.5) 0.43 (0) 0.64 (1.8) 0.64 (1.8)2423 0.38 (2.7) 0.62 (1.6) 1.4 (2.2) 1.29 (1.3) ND2425 0.35 (2.8) 0.44 (1.3) ND 0.38 (2.7) ND2426 0.29 (2.3) 0.40 (1.7) 0.48 (1.8) 0.44 (2.1) ND2427 0.36 (2.7) 0.30 (1.6) 0.40 (1.7) 0.67 (1.7) ND2428 0.25 (2.2) 0.36 (1.4) 0.35 (1.3) 0.52 (1.6) ND2448 0.36 (3.4) 0.44 (1.7) 0.31 (3.8) 1.28 (2.6) NDND, not detected. Each aggregate was counted as one particle. Table 5. Geometric mean (GSD) particle diameters(µm) for individual particles in aggregates in sam-ples of lungs from Mexico City and Vancouver.Carbon + Sample Carbon Agg sulfur AggMexico2416 0.073 (1.1) ND2417 0.077 (3.6) 0.12 (1.0)2418 ND 0.25 (1.0)2419 0.073 (2.9) 0.097 (2.7)2420 0.054 (1.0) 0.090 (2.5)2423 0.12 (1.9) 0.17 (1.7)2425 0.069 (1.7) ND2426 0.046 (2.8) 0.075 (2.1)2427 0.049 (1.9) 0.058 (1.9)2428 0.027 (1.3) 0.047 (1.9)2448 0.038 (2.3) 0.019 (1.0)Vancouver2461 ND 0.041 (1.0)aND, not detected. aOnly one aggregate identified. a link between ambient particle concentra-tions and a measure of biologically relevantdose, they support the biological plausibilityof adverse health effects being associated withexposure to particulate air pollution.REFERENCES AND NOTES1. Dockery DW, Pope CA. Acute respiratory effects of partic-ulate air pollution. Ann Rev Public Health 15:107–132 (1994).2. Vedal S. Ambient particles and health: lines that divide. JAir Waste Manag Assoc 47(5):551–581 (1997).3. Dockery DW, Pope CA, Xu X, Spengler JD, Ware JH, FayME, Ferris BG, Speizer FE. An association between airpollution and mortality in six U.S. cities. N Engl J Med329:1753–1759 (1993).4. Pope CA, Thun MJ, Namboodiri MM, Dockery DW, EvansJS, Speizer FE, Heath CW. Particulate air pollution as apredictor of mortality in a prospective study of U.S.adults. Am J Respir Crit Care Med 151:669–674 (1995).5. Abbey, DE, Nishino N, McDonnell WF, Burchette RJ,Knutsen SF, Lawrence Beeson W, Yang, JX. Long-terminhalable particles and other air pollutants related tomortality in nonsmokers. Am J Respir Crit Care Med159:373–382 (1999).6. Seaton A, MacNee W, Donaldson K, Godden D.Particulate air pollution and acute health effects. Lancet345:176–178 (1995).7. Oberdorster G, Ferin J, Gelein R, Soderholm SC,Finkelstein J. Role of the alveolar macrophage in lunginjury:studies with ultrafine particles. Environ HealthPerspect 97:193–199 (1992).8. Ferin J, Oberdorster G, Penney DP. Pulmonary retentionof ultrafine and fine particles in rats. Am J Respir CellMol Biol 6:535–542 (1992).9. Churg A. The uptake of mineral particles by pulmonaryepithelial cells. Am J Respir Crit Care Med 154:1124–1140(1996).10. Churg A, Brauer M. Human lung parenchyma retainsPM2.5. Am J Respir Crit Care Med 155:2109–2111 (1997).11. Churg A, Wright JL, Stevens B. Exogenous mineral parti-cles in the human bronchial mucosa and lungparenchyma. I. Nonsmokers in the general population.Exp Lung Res16:169–175 (1990).12. Churg A, Brauer M, Vedal S, Stevens B. Ambient mineralparticles in the small airways of the normal human lung.J Environ Med 1:39-45 (1999).13. Vedal S, Brauer M, Hernandez E, White R, Petkau J. A taleof two cities: air pollution and mortality in Mexico City andVancouver, BC. In: Proceedings of ParticulateMethodology Workshop, University of Washington,Seattle, WA, 19–22 October 1998. Seattle, WA:The NationalResearch Center for Statistics and the Environment, 1998. 14. Harrison R, Jones M, Collins G. Measurements of thephysical properties of particles in the urban atmosphere.Atmos Environ 33:309–321 (1999).Articles • Air pollution and retained particlesEnvironmental Health Perspectives • VOLUME 109 | NUMBER 10 | October 2001 1043

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