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Atmospheric Environment 77 (2013) 959e967

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Atmospheric Environment

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Particle-induced oxidative damage of indoor PM10 from coal burninghomes in the lung cancer area of Xuan Wei, China

Longyi Shao a,*, Ying Hu a, Jing Wang a, Cong Hou a, Yuanyuan Yang a, Mingyuan Wub

a State Key Laboratory of Coal Resources and Safe Mining, College of Geoscience and Surveying Engineering,China University of Mining and Technology (Beijing), Beijing 100083, Chinab School of Management, Shanghai University of Engineering Science, Shanghai 201620, China

h i g h l i g h t s

� Xuanwei is rural area in southeastern China, with a super-high lung cancer rate.� Indoor PM10s in the high lung cancer village have higher toxicity.� The heavy metals cause the toxicity of indoor PM10s in the lung cancer village.

a r t i c l e i n f o

Article history:Received 2 October 2012Received in revised form9 May 2013Accepted 31 May 2013

Keywords:Xuan WeiLung cancerPM10

Oxidative damageTrace element

* Corresponding author.E-mail address: ShaoL@cumtb.edu.cn (L. Shao).

1352-2310/$ e see front matter � 2013 Published byhttp://dx.doi.org/10.1016/j.atmosenv.2013.05.079

a b s t r a c t

The lung cancer mortality rate in the rural area of the Xuan Wei, Yunnan, is among the highest in China,especially in women. In this paper, the coal-burning indoor and corresponding outdoor PM10 sampleswere collected at the Hutou village, representing the case of high lung cancer rate, and the Xize village,representing the case of low lung cancer rate. Plasmid scission assay was used to investigate the bio-reactivity of the PM10. The inductively coupled plasma-mass spectrometry (ICP-MS) was employed toinvestigate the trace element compositions of the PM10. The results showed that the oxidative damagecaused by both indoor and outdoor PM10 at the Hutou village was obviously higher than that at the Xizevillage, with the indoor PM10 having higher oxidative damage than corresponding outdoors. Among allanalyzed samples, the indoor night PM10 samples from the Hutou village have the highest oxidativecapacity. The levels of total water-soluble elements had a higher level in the PM10 of the Hutou villagethan that of the Xize village. It is interesting that the levels of water-soluble As, Cd, Cs, Pb, Sb, Tl and Zn inPM10 had better positive correlation with DNA damage rates, implying that these elements in theirwater-soluble state should be one of the main factors responsible for the high oxidative capacity of PM10,

thus possibly the higher lung cancer rates, at the Hutou village.� 2013 Published by Elsevier Ltd.

1. Introduction

In rural Xuan Wei County, Yunnan Province, the lung cancermortality rate is among the highest in China, especially in women(27.95 and 24.49 per 100,000 for males and females, respectively)(Mumford et al., 1987). To understand the etiology of lung cancerrevealed in this unusual pattern of Xuan Wei, multidisciplinarystudies have been conducted since the late 1970s (He et al., 1995;He, 2001; Chuang et al., 1992a, 1992b; Lan et al., 1993; Lan andHe, 2004; Zhang and Smith, 2007). Many important findings haveshown that lung cancer mortality in Xuan Wei was highly associ-ated with the domestic use of bituminous coals (Mumford et al.,1987; He and Yang, 1994; Lan et al., 2002). More than 20 years’

Elsevier Ltd.

studies by He and Yang (1994) revealed that the main risk factor forthe high lung cancer mortality in XuanWei was the exposure to thehigh levels carcinogenic polycyclic aromatic hydrocarbons (PAHs)(e.g., BaP) from indoor smoky coal emissions. More recently, Tian(2005) and Tian et al. (2008) reported that the exposure variableassociated with the lung cancer risk in XuanWei was the indoor airemissions of crystalline silica. A study carried by Large et al. (2009)revealed that high silica content in coal from XuanWei County maybe interacting with toxic volatiles in the coal to cause unusuallyhigh rates of lung cancer.

It is known that during the process of coal combustion, a greatdeal of PM10 is produced and a significant amount of harmful ele-ments associated with PM10 are emitted (Wang et al., 2004; BéruBéet al., 2004), causing great harm to human health. By studying theoxidative damage of indoor and outdoor PM10s in urban Beijing,Shao et al. (2007a) reported that the PM10 generated in kitchens

L. Shao et al. / Atmospheric Environment 77 (2013) 959e967960

was the most toxic. Many epidemiology surveys have shown thatlong-term exposure to PM10 is associated with an increased risk oflung cancer (Beeson et al., 1998; Pope et al., 2002).

There are many hypotheses on the mechanisms causing pul-monary damage by particulate matter. A widely accepted hypoth-esis is that the bioavailable transitionmetals on particle surface willproduce free radicals which play an important role in causingoxidative damage (Donaldson et al., 1996; Costa and Dreher, 1997;Dreher et al., 1997; Pritchard et al., 1996; Tong et al., 2001). Bystudying free radicals of carbon black and ultrafine carbon blackwith or without transition metals, Wilson et al. (2002) demon-strated that transition metals on PM10 surface could induce pul-monary damage and had the pro-inflammatory effects. By anin vitro method, McNeilly et al. (2004) found that water-solubletransition metals could cause the pro-inflammatory effects.Richards et al. (1989) and Adamson et al. (2000) identified solublezinc in airborne particles as the reactive species causing pulmonarycell damage. Wang et al. (1999) reported that Fe was the typicaltransition metal in inducing oxygen process. So far, Zn and Fe arebelieved to be the two main transition metals responsible for theoxidative damage by PM10.

In Xuan Wei, the indoor PM10 pollution has been investigated(He and Yang, 1994) and a similarly high mass level of PM10 in bothhomes using bituminous coal (24.4� 3.3 mgm�3) and homes usingwood (22.3� 2.0 mgm�3) was reported (Mumford et al., 1987), butits relationship with the high lung cancer rates was not paidenough attention (Tian, 2005). The free radical intensity in theparticles from the combustion of the bituminous coal in Xuan Weiwas recorded to be about 10 times that found in ambient air par-ticles in other Chinese cities, and 100 times that from main streamtobacco smoke (Zhou et al., 1990). A preliminary study conducted inHutou village, Xuan Wei County, a highest lung cancer village, hasshown that the water-soluble metals such as Zn, Cd and Pb could bethe most important components responsible for the higher oxida-tive capacity of indoor PM10 in the Hutou Village (Shao et al.,2007b). In view of this, toxicity of PM10 in the indoor homes fromXuan Wei can be assessed by investigating the oxidative damagegenerated by particle-induced free radicals.

The present paper reports on the study of the oxidativedamage to plasmid DNA by PM10 collected in a high lung cancermortality village and a low lung cancer mortality village in XuanWei. Trace element contents of PM10 were examined by Induc-tively Coupled Plasma Mass Spectrometry (ICP-MS). The aims ofthis paper are to assess toxicity of PM10 and the relationship of

Table 1PM10 Sample information.

Number Site Sampling date Day or night

1 Hutou Village indoor, Home 1 2007.02.02 Day2 Hutou Village indoor, Home 1 2007.02.04 Day3 Hutou Village indoor, Home 2 2007.02.03 Day4 Hutou Village indoor, Home 1 2007.02.03w04 Night5 Hutou Village indoor, Home 1 2007.02.02 w 03 Night6 Hutou Village indoor, Home 2 2007.02.04 w 05 Night7 Hutou Village indoor, Home 2 2007.02.05 w 06 Night8 Xize Village indoor, Home 1 2007.02.09 Day

Two samples 2007.02.109 Xize Village indoor, Home 2 2007.02.10 Day10 Xize Village indoor, Home 2 2007.02.11e02.12 Night11 Hutou Village outdoor 2007.02.07 Day12 Hutou Village outdoor 2007.02.06 w 07 Night13 Hutou Village outdoor 2007.02.07 w 08 Night14 Hutou Village outdoor 2007.02.08e02.09 Night15 Xize Village outdoor 2007.02.13 Day

Two samples 2007.02.1216 Xize Village outdoor 2007.02.12e13 Night

lung cancer with the main transition metal compositions of theseinhalable particles.

2. Sampling and experiments

2.1. Sampling

There is a long history for the local residents to use the opencoal-firing stoves. The main body of the stove is buried in theground and the upper part is open to the air. Because no ventilationthe airborne inhalable particles emitted by this kind of stovescan reach a very high mass concentration level, such as24.4 � 3.3 mg m�3 (Mumford et al., 1987). Since 1973, the gov-ernment has helped local residents to rebuild the stoves, and manyXuanWei residents have begun to change fromunvented fire pits toportable stoves, or stoves with the ventilation though the under-ground chimney pipe (Tian, 2005). For those households using coal,around 6e8 tons of coal is consumed each year per household(Jiang et al., 1994).

We have carried on a sampling campaign in the Xuan Wei areaduring winter 2006/2007. The indoor and outdoor PM10 sampleswere collected at Hutou and Xize villages in the XuanWei area from1st to 25th February 2007. Hutou Village represents the high lungcancer mortality case, and Xize Village, having low or no lung cancermortality, is taken for comparison. These two villages are around30 km apart. At the Hutou village, indoor PM10 samples werecollected in the living roomsof twohouses inwhichboth familiesusebituminous coal in a ventilated fixed stove for cooking and a buriedventilated stove for cooking and heating, while at the Xize village,indoor PM10 samples were collected in the living rooms of twohouses in which farmers uses anthracite coal and wood for cookingand heating. The corresponding outdoor PM10 samples were alsocollected at the nearby localities. The daytime and nighttime sam-ples were separately collected. Negretti selective heads and poly-carbonate filters (47 mm diameter, 0.67 mm pore size, Millipore, UK)were used to collect PM10 at a flow rate of 30 L min�1. The samplingpoints were at the breathing zone (1.5 m above the floor). Informa-tion on temperature, relative humidity, pressure, wind speed andwindow opening frequency was recorded during the sampling.

A total of 16 PM10 samples were collected in the Xuan Wei area,in which 11 samples were from two houses in Hutou Village (7 in-door samples and 4 outdoor samples) and 5 samples were from twohouses in Xize Village (3 indoor samples and 2 outdoor samples).The detailed sample information is shown in Table 1.

Time: Start tofinish

Temperature/�C Relativehumidity/%

Mass/mg�1 m�3

10:30 w 18:20 8.3 64.9 126.811:00 w 18:00 10.6 65.5 115.810:40 w 17:30 10.4 61.6 103.417:40 w 10:40 9.3 60.7 151.818:30 w 10:20 9.1 63.4 63.718:20 w 14:20 12.6 58 92.520:00 w 9:30 13.2 58.1 124.914:16 w 18:46 12.5 57.9 57.610:20 w 16:30 12.6 62.1 70.809:10 w 10:10 11.4 61 277.818:00 w 9:30 14.4 53.8 102.810:00 w 17:30 14.9 40.8 39.119:15 w 9:55 5.4 76.1 42.919:00 w 09:25 5.3 72.8 57.218:10 w 9:10 5.7 72.2 39.909:00 w 18:00 22.3 31.8 21.410:00 w 12:30 20 35.5 51.9818:30 w 09:00 10.3 50.2 21.03

Table 2Average mass concentration of PM10 collected indoors and outdoors of Hutou andXize village.

Sampling sites Day average of mass levels of PM10 (�StandardDeviation) (mg m�3)

Indoor Outdoor Indoor/Outdoor（I/O）

Hutou Village 105.9 � 23.9 40.9 � 7.8 2.6Xize Village 55.9 � 14.4 23.3 � 2.7 2.4

L. Shao et al. / Atmospheric Environment 77 (2013) 959e967 961

2.2. Plasmid scission assay

Plasmid scission assay is an in vitro method of assessing andcomparing the oxidative capacity of inhalable particles (Greenwellet al., 2002; Shi et al., 2004; Shao et al., 2005). The principle of theassay is that any free radicals associated with particle surfaces candamage the supercoiled plasmid DNA by “nicking” the strands. Thisinitially causes the DNA to unwind from the supercoiled into arelaxed coil. Further damage results in linearization followed bycomplete fragmentation. This change in structure alters the elec-trophoretic mobility of the DNA, thus allowing separation andquantification on an agarose gel. The detailed experimental pro-cedure has been described in Shi et al. (2004) and Shao et al. (2005).Control samples were incubated in water. All incubations werecarried out to a final volume of 20 ml, each containing 200 ngfX174-RF DNA (Promega, London, UK). Incubations were gentlyagitated for 6 h at room temperature to ensuremaximummixing ofthe sample and to avoid sedimentation. Bromophenol blue/glycerolloading dye (3.5 ml) was added to each sample before loading. Thegels, composed of 0.6% agarose and 0.25% ethidium bromide, wererun in a 30 V electrophoretic voltage for 16 h at room temperaturein 1% tris-borate-EDTA (TBE) buffer. The finished gels were photo-graphed and the densitometric analysis was performed using theGenetools program (Syngene Systems, UK). A semi-quantitativeprotocol was established, measuring the relative proportion ofdamaged DNA (relaxed and linearized) in each lane of the gel interms of a percentage of the total DNA in each lane. Two replicatesof each lane were quantified in this way and the means wereplotted against particle concentration. Subtracting the damagecaused by the negative control (water), the DNA damage induced byairborne particles could be calculated. In order to make a compar-ison of damage rates for different samples, the damage percentageswere recorded under five scales of dosages for each sample; being25, 50, 100, 300, 500 mg mL�1. Using a linear regression, the TD50(toxic dose causing 50% damage to DNA) was calculated, and alower TD50 means a higher oxidative capacity. In this study, thewater solution of the whole sample (intact whole particle solution)and the water-soluble fraction of the particles were prepared andthe Plasmid scission assay was carried on the two kinds ofsolutions.

2.3. ICP-MS analysis

The collected PM10 samples were separated into whole and sol-uble fractions to be chemically analyzedusing a ThermoElemental XSeries (X7) ICP-MS. The mass on the polycarbonate filters wasdetermined gravimetrically. The soluble sample was obtained afteragitating the whole sample diluted in HPLC grade water in a vortexmixer (Scientific Industries, Vortex Genie 2) set at level 3 for an hourfollowed by a 10,000� g centrifugation for another hour. At the endof this stage, the supernatant (soluble fraction) was carefullyremovedusing apipette. The solution ofwhole sample (500mgeach)was prepared by digesting another quarter of filter using concen-trated nitric acid (Fisher Primar grade-specific gravity 1.48). Di-gestions were carried out in a CEMMDS-200 microwave system,using CEM advanced composite vessels with Teflon liners. Thedigested samples were then concentrated by evaporating the nitricacid and by re-dissolving in 2 ml of 10% nitric acid. Samples werediluted to a 20 ml volume using demonized (>18 MU) water. Onemilliliter of each sample was combined with a 50 ppb thalliumstandard (1 ml) and this solution was made up to 10 ml with 2%nitric acid to be analyzed in the ICP-MS. In this study, As, Cd, Co, Cr,Cs, Cu, Fe, Mn, Ni, Pb, Sb, Sn, Sr, Rb, Tl, and Zn, were measured. Thefinal results were reported as the ppm of each element and theircorresponding soluble elements in the analyzed PM10.

3. Results

3.1. Mass levels of the indoor and outdoor PM10 collected at theHutou and Xize villages

The mass levels of the indoor and outdoor PM10 at the Hutouand Xize villages were monitored during our sampling period(Table 1). There is a difference for the mass levels of indoor PM10between the Hutou and Xize villages. The indoor PM10 mass levelsat the Hutou village range from 72.7 mg m�3 w 130.2 mg m�3,averaged 105.9 mg m�3, while the indoor PM10 mass levels at theXize village range from 39.5 mg m�3 w 66.6 mg m�3, averaged55.9 mg m�3. For these daily averages, it can be seen that the indoorPM10 mass levels of the Huton village were obviously higher thanthose of the Xize Village (Table 2).

Similar to the indoor PM10 levels, the outdoor PM10 mass levelsare interesting as well. The outdoor PM10 mass levels at the Hutouvillage range from 32.3 mg m�3 w 47.5 mg m�3, averaged40.9 mg m�3, while the outdoor PM10 mass levels at the Xize villagerange from 20.2 mg m�3 w 25.2 mg m�3, averaged 23.3 mg m�3. Thedaily averages of outdoor PM10 mass levels of the Huton village areclearly higher than those of the Xize Village (Table 2).

A considerable difference exists between the mass levels of theindoor and outdoor PM10 for both sampling sites. The ratios of in-door and outdoor PM10mass concentrations, i.e. I/O ratios, are oftenused to assess the relationships between indoor air and outdoor air(Li and Chen, 2003; Monn et al., 1997; Chao and Cheng, 2002;Dimitroulopoulou et al., 2001; Lioy et al., 1990). The I/O ratiohigher than 1 indicates that the indoor PM10 is mainly sourcedindoors, in contrast, the I/O ratio lower than 1 indicates that theindoor PM10 is mainly sourced outdoors. The I/O ratios for bothHutou and Xize villages are higher than 1, being 2.6 and 2.4,respectively (Table 2), implying that the indoor activities are themajor source for generating the indoor particles.

3.2. Oxidative capacity of the PM10 collected in the Hutou and Xizevillages

The oxidative capacity of indoor and outdoor PM10 was exam-ined with the plasmid scission assay. A total of 16 PM10 samples, ofwhich the detailed information is shown in Table 1, were used inthis study. The gel images were shown in Fig. 1 and the semi-quantitative analysis of oxidative DNA damage induced by PM10from indoors and outdoors at five doses (25, 50, 100, 300,500 mg mL�1) is shown in Table 3. The TD50 values of each samplewere calculated using a linear regression (Table 3).

The PM10 from the indoor living room at the Hutou Village has aTD50 value ranging from 25 to 500 mg mL�1, averaged 182 mg mL�1,while the TD50 value of PM10 from the indoor living room at theXize Village ranges from 700 to more than 1000 mg mL�1 (Table 3).The oxidative capacity of the indoor PM10 from the homes at theHutou Village is obviously higher than that of the Xize Village. Thissuggests that the higher lung cancer rate at the Hutou village isclearly associated with highly oxidative indoor PM10.

Fig. 1. Gel image showing oxidative damage on supercoiled DNA induced by (a) indoor PM10 collected at Hutou Village during night time (No. 4); (b) indoor PM10 collected atHutou Village during day time (No. 1); (c) outdoor PM10 collected at the Hutou Village during night time (No. 13); (d) indoor PM10 collected at Xize Village during night time (No.10); (e) outdoor PM10 collected at the Xize Village during night time (No. 16); H2O is used as the negative controls. W: Whole particle solution; S: Soluble fraction.

L. Shao et al. / Atmospheric Environment 77 (2013) 959e967962

In the Hutou village, the indoor PM10 has a TD50 value rangingfrom 25 to 500 mg mL�1, averaged 182 mg mL�1, and the corre-sponding outdoor PM10 has a TD50 value ranging from 200 to800 mg mL�1, averaged 450 mg mL�1 (Table 3). The TD50 values ofindoor PM10 are clearly lower than those of the outdoor’s, indi-cating that the indoor PM10 has a higher oxidative capacity thanthat of the corresponding outdoors.

Still at the Hutou Village, a difference is noticed between theoxidative capacities of the indoor PM10 samples for the daytime andthe nighttime. The TD50 value of indoor nighttime PM10 rangesfrom 25 to 120 mg mL�1, averaged 74 mg mL�1, while the TD50 valueof indoor daytime PM10 ranges from 80 to 500 mg mL�1, averaged327 mg mL�1 (Table 3). The oxidative capacities of the indoornighttime PM10 samples are slightly higher than those of the day-time. One possible explanation could be that all doors andwindowswere tightly closed during nighttime and the harmful substanceemitted from “smoky” coal combustion can be highly enriched ontothe airborne particles.

Interesting phenomena also exist for the outdoor samples. Theoutdoor PM10 at the Hutou Village has an obviously higher oxida-tive capacity than that of the Xize Village. The TD50 values of theoutdoor PM10 at the Hutou Village is averaged 450 mg mL�1, whichis lower that of the outdoor PM10 at the Xize Village (700 to morethan 1000 mg mL�1) (Table 3).

In summary, the inhalable particles collected at both indoor andoutdoor, daytime and nighttime, the Hutou Village collections have

a general higher bioreactivity compared with the correspondingXize Village collections. The indoor night PM10 samples at theHutou Village have a highest oxidative capacity.

3.3. Trace elements in the PM10 collected in the Hutou and Xizevillages

To study the source of oxidative capacity of indoor airborneparticles in XuanWei, we have separated the soluble fractions fromintact whole solutions of the PM10 samples. The concentrations ofthe trace elements in the soluble fractions as well as in themicrowave-digested solution of intact whole samples using ICP-MSwere measured, and the results were reported as the ppm of eachelements and their corresponding soluble elements in the analyzedPM10. The elements measured include As, Cd, Co, Cr, Cs, Cu, Fe, Mn,Ni, Pb, Rb, Sb, Sn, Sr, Tl, and Zn. The results are shown in Tables 4and 5.

The concentrations of whole Cr, Fe and Sn were much higher(Table 4) than those of the corresponding soluble elements, sug-gesting that these elements exist in highly insoluble state in PM10.Other elements, such as Cd, Cs, Cu, Mn, Ni, Pb, Tl and Zn, have ahigher soluble proportion, indicating a higher solubility (Table 5).

In general, most water-soluble elements have a higher concen-tration in the indoor PM10 of the Hutou Village, compared withthose of the Xize Village. It can be seen that the total analyzedwater-soluble elements have an obviously higher concentration in

Table 3Quantification of oxidative DNA damage induced by indoor and outdoor PM10 atHutou Village and Xize Village.

Dosage(mg mL�1)

DNA damage rates of indoor PM10 at Hutou Village (%)

1W 1S 2W 2S 3W 3S 4W 4S

500 71.62 55.39 58.07 40.49 51.55 41.49 71.89 56.92300 68.64 52.95 47.54 36.96 45.17 39.04 73.47 63.17100 54.86 49.47 42.93 33.91 38.33 37.77 61.67 57.7550 47.28 45.89 38.61 25.02 34.01 31.65 46.30 43.7225 46.13 44.33 29.58 15.81 31.01 22.42 40.40 33.11TD50

(mg mLL1)80 100 400 600 500 600 75 75

Dosage(mg mL-1)

DNA damage rates of indoor PM10 atHutou Village (%)

DNA damagerates of indoorPM10 at XizeVillage (%)

5W 5S 6W 6S 7W 7S 8W 8S

500 76.75 63.82 72.54 51.86 70.21 62.47 28.05 26.08300 64.28 59.00 59.69 48.25 60.70 46.61 28.52 26.08100 63.13 58.40 58.25 47.87 48.74 41.51 26.92 26.3750 54.56 49.55 45.22 42.21 43.50 40.50 24.25 24.2525 50.43 47.42 45.65 41.95 41.18 39.52 23.34 21.91TD50

(mg mLL1)25 50 75 400 120 400 1000 1000

Dosage(mg mL�1)

DNA damage rates of indoorPM10 at Xize Village (%)

DNA damage rates of outdoorPM10 at Hutou Village(%)

9W 9S 10W 10S 11W 11S 12W 12S

500 38.96 28.09 42.41 36.91 38.46 27.41 63.76 46.47300 38.02 27.08 41.27 36.47 32.41 24.45 43.03 44.59100 32.56 25.36 32.48 35.95 27.13 19.62 41.47 41.3050 28.76 24.52 30.93 24.99 24.28 18.29 39.95 37.9925 25.14 23.66 30.25 24.49 23.39 14.78 36.24 30.53TD50

(mg mLL1)700 900 700 800 800 1000 400 500

Dosage(mg mL�1)

DNA damage rates of outdoorPM10 at Hutou Village (%)

DNA damage rates of outdoorPM10 at Xize Village (%)

13W 13S 14W 14S 15W 15S 16W 16S

500 52.53 44.45 57.27 47.64 40.64 31.78 24.82 17.60300 48.23 40.75 53.93 47.25 36.30 29.68 17.50 17.90100 42.18 38.86 47.14 46.53 33.93 24.73 10.08 8.9550 38.83 37.22 46.53 45.46 24.22 22.69 5.00 4.5625 35.60 35.75 41.96 38.85 21.54 22.34 5.08 7.81TD50

(mg mLL1)400 600 200 600 700 900 1500 1500

Table

4Th

eco

ntents

oftraceelem

ents

inthePM

10samplesfrom

theHutouan

dXizevilla

gesof

Xuan

wei

Cou

nty

(inppm).

Metals

ThewholePM

10samplesfrom

Hutouvilla

geTh

ewholePM

10samplesfrom

Xizevilla

ge

Indoo

rOutdoo

rIndoo

rOutdoo

r

No.

1No.

2No.

3No.

4No.

5No.

6No.

7No.

11No.

12No.

13No.

14No.

8No.

9No.

10No.

15No.

16

As

127.2

421

2724

213.1

871

371

488

3965

2030

93.9

235

1049

2787

460.5

313

569.6

Cd

1013

8.3

859

537

1156

.141

2312

6834

7634

489

4.5

812.4

467

39.4

119

25.8

136

95.1

Co

9.2

5.13

5.23

13.3

5.8

6.2

6.1

8.95

17.6

176.84

2.7

3.5

143.72

8.73

Cr

110.9

145

895

44.6

308

118

159

1340

155.5

85.5

84.8

344

911

64.1

231

195.4

Cs

165.81

3.16

10.7

124.6

4.2

4.18

14.3

20.7

5.6

0.9

1.3

2.7

1.94

4.17

Cu

402.7

8712

014

5.3

181

100

88.8

93.5

221.2

208.9

84.4

39.8

62.7

70.5

55.5

147.3

Fe49

1995

7116

,086

11,041

.311

,398

12,699

10,891

35,820

1447

8.5

14,486

13,859

6376

1049

514

,712

12,170

15,264

Mn

1130

.255

238

888

4.3

1313

626

698

627

6383

.442

26.1

2591

98.2

229

272.4

159

517.2

Ni

187.1

82.3

97.4

75.3

103

47.1

40.6

98.4

127.9

116.4

38.8

47.6

72.9

30.7

57.6

186.9

Pb65

90.4

1770

738

3294

.632

2026

2320

4311

6377

35.2

8293

.625

6413

112

664

9.6

556

559.5

Rb

96.5

31.2

29.8

58.2

44.8

2734

.849

.513

2.3

105.4

33.1

2539

.125

.230

.536

.5Sb

70.3

2516

47.7

44.1

34.7

11.2

22.1

44.4

62.3

35.5

5.3

6.3

16.4

12.1

39.1

Sn77

.212

8215

8540

.398

912

7890

657

5260

.495

.711

6974

131

0220

.412

702.22

Sr34

.224

.836

.846

.136

.936

.138

.711

968

.464

.834

.325

.855

.130

.928

.811

1.4

Tl25

9.1

51.5

21.2

31.9

92.1

31.3

16.6

7.77

5052

.216

.41.2

1.9

2.2

3.53

5.18

Zn26

133.7

7289

4552

14,928

16,583

16,485

16,916

6234

34,383

23,637

16,622

947

1693

508.6

1941

5089

Total

50,302

2220

1.74

2783

4.59

3203

0.8

3932

4.7

35,755

35,818

5564

8.4

6679

6.6

5237

7.9

3784

6.74

9873

.919

704.8

16,906

1696

9.69

2283

1.3

L. Shao et al. / Atmospheric Environment 77 (2013) 959e967 963

the Hutou Village than in the Xize Village, both for the indoor andoutdoor PM10 collections (Tables 4 and 5).

It can also be seen that As, Cd, Cs, Pb, Sb, Tl and Zn, havenoticeably higher concentrations both in the whole PM10 samplesand in soluble fractions from the Hutou Village, compared with thecorresponding values from the Xize Village (Tables 4 and 5).

4. Discussions

4.1. Comparison of oxidative capacity of intact whole samples andthe soluble fractions

It is widely considered that lung toxicity of atmospheric parti-cles mainly comes from water-soluble fraction (Richards et al.,1989; Adamson et al., 2000; Donaldson et al., 1997; Valavanidiset al., 2000; Ambroz et al., 2000), although Ghio et al. (1999) andImrich et al. (2000) showed that it is the insoluble fraction in at-mospheric particles that causes the biological responses of alveolusmacrophage.

To study the source of bioreactivity of the airborne particles, thesolutions before and after centrifugal separation were simulta-neously tested with the plasmid scission assay. The results show

Table

5Th

eco

ntents

ofwater-solubletraceelem

ents

inthePM

10samplesfrom

theHutouan

dXizevilla

gesof

Xuan

wei

Cou

nty

(inppm).

Metals

ThesolublePM

10samplesfrom

HutouVillag

eTh

esolublePM

10samplesfrom

XizeVillag

e

Indoo

rOutdoo

rIndoo

rOutdoo

r

No.

1No.

2No.

3No.

4No.

5No.

6No.

7No.

11No.

12No.

13No.

14No.

8No.

9No.

10No.

15No.

16

As

BL

27.6

20.6

66.4

41.7

39.8

13.2

18.8

69.9

BL

41.3

5.43

2.99

14.3

7.49

6.7

Cd

7070

.855

833

870

827

6284

322

6884

581

475.4

281

12.6

22.8

6.02

56.1

23.4

Co

3.9

1.4

1.5

3.18

1.28

1.07

1.06

1.23

3.82

5.51

1.39

0.90

60.54

1.38

1.12

3.13

Cr

3.5

4.1

4.78

3.26

5.97

3.37

3.21

3.8

6.79

4.17

4.34

5.15

0.35

2.17

7.98

3.86

Cs

10.7

3.95

2.3

7.5

8.37

3.17

2.89

1.87

10.6

13.6

3.53

0.5

0.61

1.03

0.99

1.34

Cu

257.6

12.4

14.1

23.7

33.9

10.5

7.6

5.78

33.9

27.1

7.17

7.06

1.86

6.69

12.5

24.1

FeBL

BL

3.61

39.2

BL

BL

BL

BL

159.3

BL

BL

BL

BL

6.9

BL

BL

Mn

763.7

324

181

577.5

744

242

417

119

3942

.718

30.8

1479

30.2

27.4

108.1

52.4

142.2

Ni

135

38.6

32.5

27.9

49.5

20.8

146.4

9719

.77.98

19.3

3.61

7.46

1816

6.4

Pb25

63.7

232

75.3

762.2

969

210

272

36.3

1251

.310

71.5

270

11.2

12.5

39.5

108

43.9

Rb

35.4

17.2

1241

.726

.115

.423

.112

.549

.558

.421

.315

.617

.119

.720

.125

Sb30

.313

9.7

17.8

18.3

16.7

4.83

6.86

15.3

22.1

18.7

3.4

1.64

3.5

6.29

18.6

Sn4.9

BL

BL

2.7

BL

BL

BL

BL

7.47

5.53

BL

BL

BL

1.83

BL

0.62

Sr15

.28.78

11.2

21.8

11.2

9.13

10.8

15.5

23.4

23.6

11.3

8.66

7.94

17.5

15.4

35.5

Tl20

5.7

36.4

15.4

24.8

60.1

21.8

11.5

3.93

35.5

35.3

10.3

0.73

0.77

1.35

1.88

1.68

Zn16

091.3

5019

2693

9673

10,489

9425

11,029

1610

21,734

13,302

9662

398

211

138.3

1112

452.4

Total

2719

1.7

6296

.43

3414

.99

1200

0.64

1522

0.42

1086

1.74

1407

8.19

1925

.97

2802

1.48

1689

4.71

1181

9.31

518.73

631

1.11

375.73

1420

.25

948.83

L. Shao et al. / Atmospheric Environment 77 (2013) 959e967964

that the difference between the TD50 values of the intact wholesample and the water-soluble fraction are mostly insignificant((Fig. 2 or Table 3) except for the No. 6, No. 7 and No. 14 samples.The difference between the oxidative DNA damage induced by theintact whole sample and the water-soluble fraction of PM10 at thehighest dosage (500mg mL�1) varies from 7 to 30%, mostly from 15to 20% (Fig. 3). All these facts confirmed that the oxidative capacityof airborne particulates is mainly derived from their water-solublefractions.

4.2. Association between the oxidative capacity and theconcentration of total analyzed water-soluble trace elements

Previous studies have showed that the toxicity of atmosphericparticles is closely related to presence of water-soluble trace ele-ments, especially Fe and Zn (Adamson et al., 2000; Hung andWang,2001; Whittaker et al., 2004; Moreno et al., 2004; Merolla andRichards, 2005; Shao et al., 2006, 2007a). In order to figure outthe main factors responsible for the high oxidative capacity of thePM10 samples from the Hutou Village, the relationship betweenpercentages of damaged DNA (as represented by TD50 values) andconcentrations of the trace elements in soluble fraction of the 16PM10 samples was analyzed. As a lower TD 50 value means a highertoxicity, the negative correlation between the concentration of awater-soluble element and the corresponding TD50 value wouldmean that the DNA damage is caused by this element (Shao et al.,2006). For this analysis, the correlation coefficients between thecontents of the water-soluble elements in whole particles (in ppm)and the DNA damage rates of intact whole samples (mg mL�1) weregiven in Table 6.

In overall, the concentrations of total analyzed water-solubletrace elements correlated negatively to the TD50 values of PM10samples, with a correlation coefficient being �0.71 (Table 5). Thissuggests that the higher oxidative capacity of the PM10 in XuanWeiis probably caused by the higher concentrations of the total water-soluble trace elements in the PM10.

The concentrations of total analyzed water-soluble trace ele-ments of The PM10 at the Hutou Village ranges from 1925.97 ppm to28021.48 ppm, which are obviously higher than those of the XizeVillage (from 311.11 ppm to 1420.25 ppm) (Table 5). This is well inagreement with that the TD50 values of PM10 samples from theHutou Village is obviously lower than those from the Xize Village.

Another surprising finding is that a positive association of theconcentrations of the total water-soluble trace elements and theoxidative capacity also exists in the outdoor samples in the XuanWei area. The concentrations of the total water-soluble trace

0

200

400

600

800

1000

1200

1400

1600

No.1 No.2 No.3 No.4 No.5 No.6 No.7 No.8 No.9No.1

0

No.11

No.12

No.13

No.14

No.15

No.16

TD

50 /

µg m

l-1

Fig. 2. A comparison between the TD50s of the intact whole solution and the watersoluble fraction of different PM10 samples in the Xuanwei area (Sample numbers referto Table 1).

0

10

20

30

40

50

60

70

80

90

No.1 No.2 No.3 No.4 No.5 No.6 No.7 No.8 No.9 No.10 No.11 No.12 No.13 No.14 No.15 No.16

DN

A D

amag

e / %

Whole

Water-soluble

Fig. 3. A comparison of DNA damage rates induced by the intact whole solution and the water-soluble fraction of PM10 at the highest dosage (500mg mL�1), (Sample numbers referto Table 1).

L. Shao et al. / Atmospheric Environment 77 (2013) 959e967 965

elements in the outdoor PM10 from the Hutou Village ranging be-tween 1925.97 and 28021.48 ppm, while the corresponding valuesfor the Xize Village are from 948.83 to 1420.25 ppm. There are twopossible explanations. Firstly, the Hutou village has a very longhistory of the domestic utilization of bituminous coals (almost 100years), therefore, the outdoor coal-smoke pollution is very serious,and harmful elements are highly enriched in the outdoor airborneparticles in much the same way as indoor particles. Secondly, themeteorological conditions during sampling periods would influ-ence physico-chemical properties of the PM10. A high level of traceelements in the outdoor night samples from the Hutou Village isalso monitored. The relative humidity values of air at the threesampling nights are all above 70% (Table 1), and the wetted parti-cles at the nighttime are easy to absorb more harmful elementsthan the daytime samples.

4.3. Association between the DNA damages and the concentrationof individual water-soluble trace elements

In order to investigate the relationships of the individual ele-ments with the DNA damages, the Pearson’s correlation coefficientsof the TD50 values with the concentrations of all analyzed water-soluble elements were further calculated (Table 6). It can be seenthat the water-soluble As, Cd, Cs, Pb, Sb, Tl and Zn showed negativecorrelation with the TD50 values of the PM10 at the 95% confidencelevel, with the coefficients being lower than the critical value�0.49(sample number ¼ 16). This means that the association of theseelements is most probably responsible for the higher oxidativecapacity of the PM10 samples at the indoor Hutou Village.

Within the analyzed elements, most noticeable was water-soluble Zn, which revealed a particularly significant negative cor-relation with the TD50 values, with a most evident correlationcoefficient (�0.72). It demonstrates that the higher water-soluble

Table 6Correlation coefficients between the contents of water-soluble elements in wholeparticles (in ppm) and the DNA damage rates (mg mL�1) for all indoor and outdoorsamples of the Hutou and Xize villages (sample number ¼ 16).

Watersolubleelements

As Cd Co Cr Cs Cu Fe Mn Ni

TD50W �0.68 �0.57 �0.18 0.00 �0.58 �0.34 �0.25 �0.29 0.04Water

solubleelements

Pb Rb Sb Sn Sr Tl Zn Total-M TD50S

TD50W �0.55 �0.33 �0.55 �0.54 0.26 �0.50 �0.72 �0.71 0.93

Total-M: Total analyzed soluble elements; TD50W: TD50 values of whole samplesolution; TD50S: TD50 values of soluble fraction.

Zn concentrations were associated with the lower TD50 values,and thus, higher oxidative capacity. The relatively high concentra-tions of the water-soluble zinc in the indoor PM10 samples from theHutou Village (2693e16091.3 ppm) (Table 5) are associated withrelatively low TD50 values (25e500 mg mL�1) (Table 3). In contrast,the relatively low concentrations of the water-soluble zinc in theindoor PM10 samples from the Xize Village (211e398 ppm) (Table 5)are associated with relatively high TD50 values (700 to more than1000 mg mL�1) (Table 3). Therefore, the higher the water-solublezinc concentration in PM10, the lower the TD50 values. This isconsistent with the results fromRichards et al. (1989) and Adamsonet al. (2000) who regard zinc to be an important element whenconsidering the oxidative capacity of PMs.

The oxidative capacity of soluble Zn has been confirmed bymany studies (Richards et al., 1989; Adamson et al., 2000; Shaoet al., 2006, 2007a). Cd and Pb have come under suspicion as oneof the factors for the lung cancer carcinogenesis. A study with maleWistar rats showed that exposure to cadmium chloride aerosolcaused a highly significant, dose-dependent increase in primarylung cancer (Glaser and Otto, 1986). Cox (2006) reported thatremoving Cd from cigarette smoke would reduce smoker risks oflung cancer by at least 10%. Combined with our study, it is believedthat water-soluble Zn, Cd and Pb could be the main factorsresponsible for the high oxidative capacity of PM10 samplescollected in the Hutou village.

Another bioavailable metal, iron, has been linked to the oxida-tive damage caused by particles (Donaldson et al., 1997;Wang et al.,1999; Ambroz et al., 2000; Valavanidis et al., 2000; Ambroz et al.,2000; Kim et al., 2001; Han et al., 2001). The ICP-MS analysisshowed that the Fe concentration in the whole particle sampleswas much higher than that in the soluble fractions of the particlesamples; the concentration of soluble Fe was near zero or belowdetection. This suggests that the iron in the PM10 of the Xuan Weiarea is mainly in an insoluble state. In addition, the relationshipbetween iron and the bioreactivity of PM10 was insignificant, andhence, iron is unlikely to be associated with oxidative potential ofthe Xuan Wei airborne particles.

5. Conclusions

(1) The indoor and outdoor PM10 samples (both the whole andsoluble fractions) collected in the Hutou Village have a higheroxidative capacity compared with the corresponding XizeVillage samples. The indoor night PM10 samples in the HutouVillage have a highest oxidative capacity.

(2) The concentrations of the total analyzed water-soluble ele-ments have an obviously higher concentration in the HutouVillage than in the Xize Village, both for the indoor and outdoor

L. Shao et al. / Atmospheric Environment 77 (2013) 959e967966

PM10 collections. The samples collected in the Hutou Village,both the whole and soluble fractions, have noticeably higherlevels of As, Cd, Cs, Pb, Sb, Tl and Zn, compared with the cor-responding samples collected in the Xize Village.

(3) The concentrations of the total water-soluble elements in theanalyzed PM10 samples show a significant negative correlationwith their TD50 values, suggesting that the elements in theirsoluble state should be the main causes responsible for thehigh oxidative capacity of the PM10 samples collected in theHutou village. Of the analyzed elements, As, Cd, Cs, Pb, Sb, Tland Zn, showed a most significant correlation with the oxida-tive capacity.

Acknowledgments

This work was supported by the National Natural ScienceFoundation of China (Grant No. 41030213), and the National BasicResearch Program of China (grant No. 2013CB228503). Kelly BéruBéis thanked for supervising the DNA assay experiments. RobertFinkelman and Zhou Yiping are thanked for helpful comments tothe initial draft of the manuscript.

Appendix A. Supplementary data

Supplementary data related to this article can be found at http://dx.doi.org/10.1016/j.atmosenv.2013.05.079.

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