Characterization of Particulate Matter Profiling and Alveolar Deposition from Biomass Burning in Northern Thailand : The 7-SEAS Study

Biomass burning (BB) frequently occurs in SouthEast Asia (SEA), which significantly affects the air quality and could consequently lead to adverse health effects. The aim of this study was to characterize particulate matter (PM) and black carbon (BC) emitted from BB source regions in SEA and their potential of deposition in the alveolar region of human lungs. A 31-day characterization of PM profiling was conducted at the Doi Ang Khang (DAK) meteorology station in northern Thailand in March 2013. Substantial numbers of PM (10147 ± 5800 # cm) with a geometric mean diameter (GMD) of 114.4 ± 9.2 nm were found at the study site. The PM of less than 2.5 μm in aerodynamic diameter (PM2.5) hourly-average mass concentration was 78.0 ± 34.5 μg m, whereas the black carbon (BC) mass concentration was 4.4 ± 2.6 μg m. Notably, high concentrations of nanoparticle surface area (100.5 ± 54.6 μm cm) emitted from biomass burning can be inhaled into the human alveolar region. Significant correlations with fire counts within different ranges around DAK were found for particle number, the surface area concentration of alveolar deposition, and BC. In conclusion, biomass burning is an important PM source in SEA, particularly nanoparticles, which has high potency to be inhaled into the lung environment and interact with alveolar cells, leading to adverse respiratory effects. The fire counts within 100 to 150 km shows the highest Pearson's r for particle number and surface area concentration. It suggests 12 to 24 hr could be a fair time scale for initial aging process of BB aerosols. Importantly, the people lives in this region could have higher risk for PM exposure.


INTRODUCTION
Carbonaceous particles, an important source emitted from biomass burning (BB), are commonly produced from the open burning of agricultural residues, slash-and-burn practices, grassland and forest fires, and residential combustion of biofuels for cooking and heating.Surfaces of these carbonaceous particles provide a platform to intermix with various chemicals such as metals and organics, which can increase the toxicity of the particles.Epidemiological evidence shows that particulate matter (PM) at levels typically found in urban areas are considered to have adverse health effects, including exacerbation of pre-existing respiratory diseases (Kumar et al., 2013;Díaz-Robles et al., 2015).For example, Kumar et al. (2013) observed that the 2.3% risk of an acute exacerbation of chronic obstructive pulmonary disease (COPD) could be increased by a unit increase in exposure to PM of less than 2.5 µm in aerodynamic diameter (PM 2.5 ).Notably, the prevalence rate of COPD in South Asia was 4.2%-9.4% as reported by Lim et al. (2015) in 2015, suggesting that characterization of PM emitted by biomass burning is urgent for public health.
PM typically reaches a peak level during the premonsoon season (March-April) in Southeast Asia, which is associated with biomass burning.Such combustion activities significantly contribute to regional PM emissions (Carmichael et al., 2009;Tsay et al., 2013Tsay et al., , 2016)).The resultant haze episodes cause significant pollution levels, such as PM, that far exceed regional air quality standards (Chew and Bhatia, 2008).The seasonal emissions peak occurs prior to the onset of the Asian summer monsoon rains and is prevalent over forested regions of the peninsula including Myanmar and northern Thailand (Lin et al., 2013).However, BB emissions in SEA have garnered less attention than those in other tropical regions (Lin et al., 2013(Lin et al., , 2014;;Lee et al., 2016).Additionally, the quantitative contribution of biomass burning in Myanmar and Thailand to levels of PM in other countries within SEA in relation to local air pollution sources remains poorly understood.
The lungs are the primary port of entry for airborne agents; therefore, clearance of deposited foreign materials from the lungs is critical for the whole-body defense.Particle size is usually categorized according to the penetrating ability into the human respiratory system.Briefly, thoracic particles (PM of < 10 µm in aerodynamic diameter) can readily penetrate and deposit in the tracheobronchial tree (BéruBé et al., 2007), whereas fine particles (PM 2.5 ) bypass the upper airways and are deposited in the lower and distal lung environments (Bai et al., 2001;Monn et al., 2003;Patterson et al., 2014).Conspicuously, considerable research has been devoted to nanoparticles that can be inhaled into the alveolar region due to their unique size fraction.Deposition sites of inhaled PM are dependent on the size and clearance time of the deposited particles, which varies depending on the deposition site (Kristensson et al., 2013).Hata et al. (2014) observed that more than 30% of combustion-derived PM from the burning of biomass fuel had a mass that fell within a range of < 100 nm.Therefore, it is important to characterize profiles of PM emitted from biomass burning in the SEA region.The objectives of this study were to: (1) characterize particulate matter (PM) and black carbon (BC) profiles and (2) estimate nanoparticles that are able to deposit in the human alveolar region.

METHODS
Physical properties, including the particle size distribution, PM 2.5 , BC mass concentration, and lung-deposited surface area of BB aerosols in SEA source region were simultaneously measured.The source-region site of the BASELInE campaign was located at the Doi Ang Khang meteorology station in northern Thailand (DAK; 19.93°N, 99.05°E, 1536 m above sea level; Fig. 1), which is about 180 km north of Ching Mai and only 300 m away from the border between Myanmar and Thailand (the two major BB sources in this region).In the neighboring area, there are no significant local industrial emission sources, and it is remote from major traffic routes.Field measurements were conducted from 1 March to 31 March 2013 (a total of 31 days), which coincided with the regional intensive BB season.
A weather transmitter (Vaisala Model WXT-520, Helsinki, Finland) logged temperature, relative humidity (RH), ambient pressure, wind speed, and wind direction at 4 m above ground during the experiment.Meteorological data were recorded in one minute time solution and averaged to 1-hour intervals for this study.The fire data from MODIS (Moderate Resolution Imaging Spectroradiometer) on board NASA's Terra and Aqua satellites provide an unprecedented record of global fire activity.In this study, the MOD14 (Terra) and MYD14 (Aqua) active fire product detects fires in 1 km pixels that are burning at the time of overpass under relatively cloud-free conditions (Giglio et al., 2003).The overpass time for Terra and Aqua are approximately 10:30 and 13:30 local time, respectively.The daily fire counts are calculated from sum of MOD14 and MYD14 data sets.
During the observation period, for ambient particle number/size distributions, a scanning mobility particle spectrometer (SMPS, TSI 3936, USA) was used to measure particles in the size range of 13.6-736.5nm.PM 2.5 mass concentrations were determined by a Tapered Element Oscillating Microbalance (TEOM, RP 1400a, USA), and BC mass concentrations were monitored with an Aethalometer (Magee AE31, USA).In addition, the lung-deposited surface area in units of micrometers squared per cubic centimeter (µm 2 cm -3 ) was observed with a TSI AeroTrak 9000 (USA).All instruments were situated in NASA's SMART (Surfacesensing Measurements for Atmospheric Radiative Transfer, cf.http://smartlabs.gsfc.nasa.gov)mobile laboratory, which provided a well-controlled and thermostatic environment.The continuous sampling inlets were all located on the roof of the SMART trailer and were at least 5 m above ground level.

Biomass Burning and PM
Lowland forests and plantations are burnt annually during the dry seasons (March-April and July-October) in South Asian areas.To monitor the ambient PM during the biomassburning period, in March, 31 days of online monitoring of PM was conducted at DAK, which is between the two major BB sources in this region (Lin et al., 2014).The average temperature was 21.6 ± 2.6C, and the relative humidity (RH) was 48.3% ± 22.1% (Fig. S1(a)).The average pressure was 839.0 ± 1.9 mbar, and wind speed was 5.6 ± 1.9 m s -1 (Fig.

S1(b))
. There was four rainy days on 4-7 March during this field campaign.Fig. 2 shows the number of fire incidents determined around the monitoring station.For the fire events counted within 200 and 500 km from DAK, the overall average numbers were 368 ± 372 and 1642 ± 1205 times with an increasing trend.The number of fire counts reached to a maximum value of 3889 on 20 March.According to a historical fire data set, the peak fire day in a year generally occurred in the middle of March.The peak date of deliberate man-made fires is mostly decided by farmer's practice beside a basic requirement on favorite weather condition.
As shown in Fig. 3(a), the daily average particle number concentrations measured with the SMPS was 10147 ± 5800 (range, 1756-21741) # cm -3 with a geometric mean density (GMD) of 114.4 ± 9.2 nm.For the particle size distribution measured by SMPS, the range of GMD was comparable to the count median diameter (CMD) centered at 130 nm for fresh smoke reported by Reid et al. (2005) and the GMD of the accumulation mode (128-190 nm) observed by Rissler et al. (2006).The high number concentration and small GMD observed in the late afternoon/evening is considered to mainly be attributed to peak fire activities (Prins et al., 1998;Rissler et al., 2006).
The mean value ± SD of PM 2.5 24hr-average mass concentration over the whole observation period was 78.0 ± 34.5 µg m -3 , and the 24hr-average PM 2.5 ranged from 18.8 (on 9 March) to 139.1 µg m -3 (on 21 March) (Fig. 3(b)).There were 16 days on which the average PM 2.5 mass concentrations exceeded 50 µg m -3 during the study period, accounting for 84% of the total measurement days (19 measurement days in total).Notably, the highest level of the PM 2.5 mass concentration was 4-fold the 24-hr PM 2.5 National Ambient Air Quality Standard of 35 µg m -3 .Similarly, a previous study measured PM 2.5 levels in eight cities in Thailand during the same study period as the present study (March 2013), and found that the highest mass concentration of PM 2.5 was 209.9 µg m -3 in Mae Hong Son with an average concentration of 85 µg m -3 (Pongpiachan et al., 2013).Chronic and/or acute exposure to such high levels of PM 2.5 concentrations in this area may increase the risk of cardiopulmonary diseases.
BC is responsible for the importance of BB-derived PM as it can effectively absorb light across the entire solar spectrum and contributes to the warming effect on the radiative budget of the earth (Jacobson, 2001;Wang et al., 2015;Sayer et al., 2016;Pani et al., 2016).Also, BC could play an important role in inhalation toxicity too (Cai et al., 2014).BC's morphology is generally fractal and porous, and is able to provide lots of reactive sites and large surfaces for many heterogeneous reactions.Since the changes of surface chemistry could potentially increase burden of toxic materials on PM (Oberdörster et al., 1995;Dye et al., 2001;Höhr et al., 2002;Latif and Brimblecombe, 2004).An association between BC and adverse human health was recently discovered (Mordukhovich et al., 2015), such as cardiopulmonary, cardiovascular, and respiratory diseases (Smith et al., 2009;Kupiszewski et al., 2013).During this campaign, the average BC concentration observed in DAK was 4.4 ± 2.6 µg m -3 (Fig. 3(b)).An Indian study observed that the spring BC level was 17.8 µg m -3 , which is higher than our finding.The difference could be due to the monitoring sites and distances to the fire sources.According to a review by Reid of carbon apportionment studies using thermal evolution techniques, the mean BC mass fraction in fresh BB particles was 8% ± 6%, and ranged 2%-27% (Reid et al., 2005).Haywood et al. (2003) also reported that the mass fraction of BC was 5% in Africa (Haywood et al., 2003).Consistently, our results show that the mass ratio between BC and PM 2.5 mass concentrations was between 5.6% and 9.4% (Fig. 3(b)).The results suggest that biomass burning was a predominant emission source during the sampling period.These high levels of PM emissions confirmed that the campaign site is certainly located in the source region of biomass burning.Although the population in this region (136.3Pop.km -2 ) is less dense than the coastal area of Indochina (Fig. 1).Children have higher potential to expose more air pollutants than adults due to children generally breathe more rapidly than adults.Additionally, children spend more time outdoors than adults, leading to prolonged pollutant exposure.Biologically, children are often more susceptible to the health effects of air pollution because their immune systems and developing organs are still immature.The other vulnerable group to air pollutants is elderly.The elderly commonly exists with respiratory or cardiac diseases, which is considered to be especially sensitive to the harmful effects of air pollution.Therefore, reduction of exposure to BB-derived PM among susceptible groups, such as elder people and young children, should be undertaken for human health protection.

Deposition of Nanoparticles in the Alveolar Region
Several studies also reported that metrics different from the currently regulated total emitted particulate mass, such as number distribution (Wittmaack, 2007) or surface area (Oberdörster et al., 2005(Oberdörster et al., , 2007;;Levin et al., 2016) could be more relevant than mass for determining some possible health-related effects, especially for nanoparticles (Burtscher, 2005;Isella et al., 2008;Löndahl et al., 2009).Therefore, to assess the potential risks of exposure to nanoparticles emitted from biomass burning in the lung environment, particularly the alveolar region, estimation of nanoparticle deposition surface area was determined using AeroTrak in this study campaign.AeroTrak is using a patented counterflow diffusion charger to bring the sampling particles to a defined charged state and the corresponding aerosol current was detected by a Faraday cup electrometer.By selecting the voltage of the "ion trap" to remove excess ions and charged aerosol, the measured currents will be proportional to the lung deposited surface area concentration in alveolar or tracheobronchial region as described by ICRP.To our knowledge, direct surface area measurements of BB aerosols have not been conducted in any previous field study.Fig. 4 shows that the surface area concentrations of alveolar deposition steadily increased to a peak level of 214.9 µm 2 cm -3 on 20 March with an average concentration of 100.5 ± 54.6 µm 2 cm -3 during the sampling period.Previous studies have shown in typical urban environments the background surface area concentrations of alveolar deposition range from 30 to 70 µm 2 cm -3 (Ntziachristos et al., 2007;Sabbagh-Kupelwieser et al., 2010).On the other hand, Wang et al. (2009) reported the ultrafine particles per alveolar deposited surface area 63 to 125 µm 2 cm -3 on road or along roadsides, and Gomes et al. (2012) found the value varies between 35 to 89.2 µm 2 cm -3 in a major avenue of Lisbon, Portugal during a typical week.Although higher measurements could be observed for traffic related emissions, the values observed in BB source region in this study is slightly higher than these reported values.Stoeger et al. (2006) indicated that the surface area is an important reference unit for assessing causative health effects of carbonaceous nanoparticles.Furthermore, an association between alveolar deposition in surface area emitted from candle burning and a change in human lung function was observed (Soppa et al., 2014).Together, pulmonary exposure to nanoparticles produced from biomass burning may increase the risk of developing pulmonary disorders.
Data provided by AeroTrak not only allowed us to study PM-related health impacts but also gave us real-time information about PM morphology in combination with the particle size distribution measured by SMPS.In the present study, we further determined the ratio of the surface area concentration of alveolar deposition to the nanoparticle number (< 100 nm as determined by SMPS) (Fig. 4).We observed that the ratio presented a significantly different trend compared to levels of surface area in alveolar deposition.The average surface area of alveolar deposition per particle (nanoparticle) was 0.025 ± 0.006 µm 2 # -1 , and ranged 0.017-0.038µm 2 # -1 .The ratio has the units of µm 2 particle -1 (nanoparticle) and can be viewed as the average nanoparticle surface area in alveolar deposition.As to fractals of burned biomass aerosols, more surface area for a single size with an identical volume equivalent indicates a greater fractal morphology of particles.Nanoparticles tend to be short-lived in the ambient atmosphere, since they agglomerate and coalesce into larger particles with variable morphologies (e.g., spheres and aggregates) (BéruBé et al., 1999;Avino et al., 2011).It should be noted that the large surface area of freshly generated nanoparticles emitted from biomass burning is not only available for condensation of water molecules but also for gases, for example organic vapors, which could have higher particle bioreactivity.

Associations of Fire Counts and PM
As reported in the literature, the particle number concentration and BC mass concentration are potential indicators of biomass burning (Zhang et al., 2015).To investigate and/or confirm the PM sources during the intensive observation period, associations of fire counts within different ranges from DAK with the particle number concentration, PM 2.5 , and BC mass concentration and the surface area concentration of alveolar deposition were evaluated in terms of the correlation coefficients (Pearson's r; Tables 1 and 2).It was observed that the optimal r for BC was settled in the range of 200 to 250 km around DAK, but the difference between BC's r-values in different ranges was relatively minor.While, for both particle numbers and the surface area concentration, the optimal rs were located in the region of 100 to 150 km around DAK and these findings echo the backward trajectory analysis using the NOAA ARL HYbrid Single-Particle Lagrangian Integrated Trajectory (HYSPLIT) model v.4 (R.R. Draxler and G.D. Rolph, 2003; HYSPLIT4 Model access via http://www.arl.noaa.gov/ready/hysplit4.html,Air Resour.Lab., Natl.Oceanic and Atmos.Admin., Silver Spring, MD.) (Supplementary Fig. S2).The air masses arrived DAK were generally from the West/ Myanmar and sampled ground emission around 12 to 24 hr before reaching DAK (100-250 km west to DAK), which is also observed in the 2015 7-SEAS/BASELInE campaign and reported by Sayer et al. (2015).However, the freshly emitted BB aerosols would experience the aging processes, such as condensation and coagulation, to transform their size distribution and particle morphology even during the short 24-hr transport.Therefore, comparing to the fairly moderate correlations for BC over a wide fire-counting range (100-250 km), the optimal high rs were found in the closer fire-counting range of 100 to 150 km around DAK for both particle numbers and the surface area concentration.In addition, this suggests that 12 to 24 hr could be a fair time scale for initial aging process of BB aerosols in SEA.Similar conclusions were also reported in the literature.Zhong and Jang (2014) concluded that the OC of BB aerosol becomes less light absorbing after 8-9 hr sunlight exposure compared to fresh wood-burning OC.The organic material could be profound in fresh BB aerosols in source region and were either photo-chemically aged or diluted by coating materials while transported.Further, the other study also suggest that fresh fractal BB aerosols residing in the atmosphere for more than 1 hr could collapse sufficiently to be considered spherical (Martins et al., 1998).These associations revealed that biomass burning is an important emission source of nano-to submicron sized PM.Although nano-to submicron sized PM are highly abundant in terms of number and surface area, they only contribute partially to the mass of the total PM.Thus, PM 2.5 only show a moderate correlation with the fire counts and the correlation decreases with the recoding distance.On the other hand, this finding indicates that a significant number of nanoparticles emitted from biomass burning in the region of the study site can be inhaled into the alveolar region.Deposition of particles in the lungs is higher in susceptible groups, which could increase particle deposition and was proportional to the severity of lung obstruction (Hazucha et al., 2013;Patterson et al., 2014).Idolor et al. (2011) showed that biomass burning contributes to the development of COPD in the Philippines.The surface area of which could be associated with increased adverse health impacts, and PM mass ought not to be the sole exposure metric when assessing the environmental and health effects of BB aerosol.Together, biomass burning in the region around DAK is an important pollutant source, the human health effects of which should be more closely monitored.

CONCLUSIONS
In conclusion, impacts of biomass burning in northern Thailand on the regional air quality were investigated in spring 2013.It was observed that enormous numbers of PM were emitted from biomass burning.Also, approximately 84% of the PM 2.5 mass concentration at DAK in the study period was > 50 µg m -3 .Very high levels of PM 2.5 were observed, which was 4-fold the 24-hour PM 2.5 National Ambient Air Quality Standard.The BC concentration was 4.4 µg m -3 .Biomass burning is an important PM emission source in the present study based on results of the BC to PM 2.5 ratio (5.6%-9.4%)and high correlations of fire counts to particle numbers, the surface area concentration of alveolar deposition and BC.The correlation coefficients (Pearson's r) with fire counts within 200 km from DAK were 0.742, 0.692, 0.615 (p < 0.001) for particle number, the surface area concentration of alveolar deposition and BC, respectively.Importantly, the present study provides surface area concentrations in the alveolar region in this field campaign for the study period.Results show that high concentrations of particle surface area (100.5 ± 54.6 µm 2 cm -3 ) emitted from biomass burning can be inhaled into the alveolar region.These nanoparticles with very fractal structure could be deposited in the deeper lung environment, leading to adverse respiratory effects.However, the different correlations for the fire counts within different ranges suggests the size distribution and particle morphology of BB aerosols could change considerably within as short as 24-hr transporting time.In other words, the total particle number and the surface area concentration of alveolar deposition could vary dramatically while the PM 2.5 still remain as it was.Therefore, PM mass may not be the proper exposure metric for assessing the health effects in the BB source regions.Additional exposure metrics, such as particle number and surface area concentration, should be included and studied as well.

Fig. 4 .
Fig. 4. Lung deposition surface area concentration in the alveolar region measured by TSI AeroTrak, and the normalized lung deposition surface area concentration per particle.

Table 1 .
Correlation coefficients (Pearson's r) between fire counts (within different distances from DAK) and total particle numbers, PM 2.5 , BC, and the surface area concentration of alveolar deposition.(The bold figure indicates the highest r among the different distances for each category.)

Table 2 .
Correlation coefficients (Pearson's r) between fire counts (within different ranges around DAK) and total particle numbers, PM 2.5 , BC, and the surface area concentration of alveolar deposition.(The bold figure indicates the highest r among the different ranges for each category.) * p < 0.05, ** p < 0.01, *** p < 0.001.