Article
pubs.acs.org/est

Impact of Natural Gas Extraction on PAH Levels in Ambient Air
L. Blair Paulik,† Carey E. Donald,† Brian W. Smith,† Lane G. Tidwell,† Kevin A. Hobbie,† Laurel Kincl,‡
Erin N. Haynes,§ and Kim A. Anderson*,†
†

Department of Environmental and Molecular Toxicology, Oregon State University, Corvallis, Oregon 97331, United States
College of Public Health and Human Sciences, Oregon State University, Corvallis, Oregon 97331, United States
§
Department of Environmental Health, University of Cincinnati, Cincinnati, Ohio 45267, United States
‡

S Supporting Information
*

ABSTRACT: Natural gas extraction, often referred to as
“fracking,” has increased rapidly in the U.S. in recent years. To
address potential health impacts, passive air samplers were
deployed in a rural community heavily affected by the natural
gas boom. Samplers were analyzed for 62 polycyclic aromatic
hydrocarbons (PAHs). Results were grouped based on distance
from each sampler to the nearest active well. PAH levels were
highest when samplers were closest to active wells. Additionally,
PAH levels closest to natural gas activity were an order of
magnitude higher than levels previously reported in rural areas.
Sourcing ratios indicate that PAHs were predominantly
petrogenic, suggesting that elevated PAH levels were influenced
by direct releases from the earth. Quantitative human health
risk assessment estimated the excess lifetime cancer risks associated with exposure to the measured PAHs. Closest to active wells,
the risk estimated for maximum residential exposure was 2.9 in 10 000, which is above the U.S. EPA’s acceptable risk level.
Overall, risk estimates decreased 30% when comparing results from samplers closest to active wells to those farthest. This work
suggests that natural gas extraction may be contributing significantly to PAHs in air, at levels that are relevant to human health.

■

INTRODUCTION

Many studies have acknowledged that impact to air quality
may be the most significant risk to communities living near
NGE.8−15 Shonkoff et al. concluded that NGE has the potential
to pose health risks through both air and water emissions, and
urged that many important data gaps remain.9
Most of the air quality studies have focused on emissions of
volatile organic compounds (VOCs). McKenzie et al. sampled
air near NGE wells at different stages, measuring VOCs
including BTEX (benzene, toluene, ethylbenzene and xylenes)
and aliphatic hydrocarbons.10 They performed a public health
risk assessment and found an increased risk of cancer and
noncancer endpoints for people living within 0.5 miles of NGE
well pads.10 In a subsequent study, McKenzie et al. assessed the
correlation between decreased birth outcomes and NGE. They
found an increase in congenital heart defects and neural tube
defects as mothers’ residences got closer to NGE wells.11 Roy
et al. estimated emissions from NGE in the Marcellus Shale,
and predicted that NGE contributes an average of 12% of all
NOx and VOC emissions to air in a given location.12 Bunch et
al. studied regional VOC levels in a part of Texas with NGE.14
Contrary to the majority of the scientific literature, this study

Natural gas extraction from shale, colloquially known as
“fracking,” has increased substantially in the United States in
the past 15 years. U.S. shale gas production grew by 17%
annually from 2000 to 2006, and then grew by 48% from 2006
to 2010.1 This spike in activity has been driven predominantly
by improvements to the technologies of horizontal drilling and
hydraulic fracturing. Together, these processes enable companies to access gas reserves previously out of reach. As of 2011,
the U.S. Energy Information Administration estimated that
roughly 750 trillion cubic feet of natural gas were recoverable
from shale reserves in the contiguous United States using these
approaches.2
Despite this rapid expansion and implementation of
technology, there has been relatively little research into the
environmental and health impacts these processes may have.
There has also been a lack of regulation, illustrated by the U.S.
Energy Policy Act of 2005, which amended portions of the U.S.
Safe Drinking Water Act and Clean Water Act to give gasdrilling companies more flexibility.3 Concerns have arisen about
the impacts that natural gas extraction (hereafter NGE) may
have on environmental and human health, due in part to this
historic lack of regulation.4−7 In the past five years, studies have
emerged assessing the impacts this activity may have on water
quality, air quality, and human health.8−20
© 2015 American Chemical Society

Received:
Revised:
Accepted:
Published:
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March 5, 2015
March 23, 2015
March 26, 2015
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leases.30 As of June 2014, that number had jumped to 1386,
with 421 in Carroll County.31
Passive air samplers were deployed on the properties of 23
volunteers in February 2014. Volunteer landowners were
identified by advertisement through a community meeting
and word of mouth. Volunteers were excluded from the study if
their properties were within a city limit, near an airport, or
otherwise could have presented results that were difficult to
interpret due to substantial background PAH levels. Each
sampling site was located between 0.04 and 3.2 miles from an
active NGE well pad. Oregon State University (OSU)
researchers deployed one sampler on each volunteer’s land.
Each sampler consisted of three LDPE strips in a metal cage.
Sampling was replicated in triplicate at one site. The OSU
research team has over 10 years of field sampling experience
collectively. The team took care to place samplers as far as
possible from potentially confounding PAH sources such as
chimneys or roads. Samplers were deployed for 3−4 weeks, and
then trained landowners mailed them to the Food Safety and
Environmental Stewardship (FSES) lab at OSU in Corvallis,
OR. Volunteer training is described further in the Supporting
Information (SI). Samplers were transported in airtight
polytetrafluoroethylene bags with Clip N Seal assemblies
(Welch Fluorocarbon). Landowners were provided individual
results from air sampling on their property. To put results in
context, individual results were compared to a summary of
results from all sampling sites.
Passive Sampler Preparation, Cleaning and Extraction. Details about chemicals and solvents are in the SI. Before
deployment, LDPE was cleaned using hexanes as described
previously.32 Each LDPE strip was infused with performance
reference compounds (PRCs) to enable calculation of in situ
sampling rates and time-integrated air concentrations.33 PRCs
used in this study were fluorene-d10, pyrene-d10 and
benzo[b]fluoranthene-d12. PRCs were spiked into LDPE at
2−20 μg per strip. Samplers were cleaned after deployment in
two isopropanol baths, stored in amber jars at −20 °C, and
extracted as described elsewhere.32 Briefly, extractions were
performed using two dialyses with n-hexane. Prior to extraction,
samples were spiked with deuterated PAHs to act as surrogate
standards, allowing for quantification of extraction efficiency.
Surrogate standards are specified in SI Table S1. Extracts were
quantitatively concentrated to 1 mL using TurboVap closed cell
evaporators, transferred to amber chromatography vials, and
stored at −20 °C.
Chemical Analysis. LDPE extracts were quantitatively
analyzed for 62 PAHs using an Agilent 7890A gas chromatograph interfaced with an Agilent 7000 GC/MS-MS. An Agilent
Select PAH column was used. Each PAH was calibrated with a
curve of at least five points, with correlations ≥0.99. Limits of
detection (LODs) range from 0.24 to 1.7 ng/mL, and limits of
quantitation (LOQs) range from 1.0 to 7.1 ng/mL, with the
exception of two compounds that have higher LODs and
LOQs. A list of PAHs, LODs and LOQs is included in SI Table
S1.
Air Concentration Calculation. Air concentrations (ng/
m3) of PAHs were calculated from instrument concentrations
(ng/mL) using PRCs. In situ sampling rates (RS) were
generated using calculations described by Huckins et al.33
These calculations estimate the R S of each PRC by
incorporating deployment time, average temperature, initial
amount and KOA. An RS is then calculated for each PAH, using

concluded that NGE is not polluting the air at concerning
levels. However, Bunch et al. considered any risk estimates less
than 1 in 10 000 not to be concerning, which is the upper limit
of risk that the EPA considers acceptable.21
Many studies have assessed the impacts of NGE on public
health.7,9−11,14,16−20,22 Colborn et al. performed a hazard
assessment of the chemicals that are used during NGE, and
concluded that over 70% of these chemicals are potentially risky
to humans.7 Other work has focused on the impacts of NGE on
communities.18,19,22 NGE often takes place in rural areas, where
it may present a larger change to ambient pollutant levels than
it would in urban areas.
Other studies have reviewed the state of the science
surrounding NGE, emphasizing the need for more concerted
field sampling and data generation. In one such review,
Goldstein et al. called for toxicological studies to help
characterize the potential risks of NGE activity.17 Small et al.
assessed the state of the science and regulation surrounding
NGE in the U.S. They called for improved characterization of
air pollutants emitted from NGE and their potential health
impacts, and concluded that risks associated with NGE “remain
under-analyzed”.6 Despite the recent surge of literature
surrounding NGE, there are still many data gaps.
One data gap is the relationship between polycyclic aromatic
hydrocarbons (PAHs) and NGE. PAHs are pervasive environmental pollutants of concern, known to be associated with both
hydrocarbon extraction and negative health impacts.23,24 The
main categories of health concerns associated with exposure to
PAH mixtures are cancer risk and respiratory distress. PAHrelated cancer risk has received a great deal of attention in
relation to oil spills, traffic exhaust, wood smoke, and cooking.
NGE involves extracting hydrocarbons from the earth, a
process that is often associated with PAH emissions. NGE also
brings large volumes of truck traffic into an area to move
building materials, water, and product. Each of these stages
could be sources of PAHs. Goldstein et al. and Adgate et al.
both specifically include PAHs as a potential health concern at
many or all stages of NGE.8,17 Colborn et al. sampled air near
NGE well pads for 16 PAHs.15 However, they ceased sampling
PAHs after the drilling phase ended. They later concluded that
PAH levels during drilling were of concern to human health,
citing that these levels (∑PAH16 ∼15 ng/m3) were comparable
to those associated with small but significant decreases in IQ at
5 years of age in children exposed in utero.25 Colborn et al.
conclude that the relationship between NGE and PAH
emissions “deserves further investigation.”15
Passive sampling could fill this data gap. Low-density
polyethylene (LDPE) passive samplers sequester hydrophobic
compounds through passive diffusion in a time-integrated
manner, and are well-suited to passively sample vapor phase
PAHs from air. Since this tool’s development in the 1990s,
many studies have demonstrated its ability to measure
PAHs.26−29 The objective of this study was to use passive
sampling to assess the impact of NGE on PAH levels in air in a
rural community.

■

MATERIALS AND METHODS
Site Description and Sampling Design. This study took
place predominantly in rural Carroll County, Ohio. As
technology has made gas in the Utica shale more accessible
in the last five years, NGE in eastern Ohio has increased. In
2011, Ohio had less than 50 horizontal natural gas drilling
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Figure 1. Average PAH concentrations grouped by distance to the closest active natural gas well. a. Sum of 62 PAHs, b. benzo[a]pyrene, and c.
phenanthrene. The three distance groups are close (n = 5), middle (n = 12), and far (n = 6), defined in the text. Error bars represent one SD. The
asterisk indicates a significant difference between the close and far groups for benzo[a]pyrene, p < 0.05.

the PAH’s KOA and the RS of one of the PRCs. These
calculations are included as SI eqs S1−S3.
Data Analysis. Data was grouped by distance from each
sampling site to the closest active well pad. Three distance
groups were created, with the “close” group <0.1 mile from an
active well, the “middle” group from 0.1 to 1.0 mile from an
active well, and the “far” group >1.0 mile from an active well.
The close, middle and far groups had 5, 12, and 6 samples each.
All results are presented in these three distance groups.
Distances were determined using Google Earth version
7.1.2.2041, and well status information was taken from the
Ohio Department of Natural Resource’s Web site. A well was
considered “active” if it was in the drilling, drilled, or producing
stages at the time of sampling.
Parent PAH isomer ratios were used to determine sources of
PAHs. Two PAH isomer pairs that are used to diagnose
whether a PAH mixture is petrogenic or pyrogenic are
phenanthrene and anthracene, and fluoranthene and pyrene.34−40 Phenanthrene/anthracene ratios ≤10 indicate pyrogenic sources, while ratios ≥15 indicate petrogenic sources.34,36−38 For this ratio, there is disagreement about
interpretation of values between 10 and 15. Budzinski et al.
state that values in this range suggest incomplete combustion of
organic matter, and are thus pyrogenic.34 Fluoranthene/pyrene
ratios >1 indicate pyrogenic sources, while ratios <1 indicate
petrogenic sources.34,37,38 Ratios of one isomer to the sum of
both isomers are also used in PAH sourcing. Fluoranthene/
(fluoranthene+pyrene) ratios ≥0.5 indicate pyrogenic sources,
and ratios ≤0.4 indicate petrogenic sources.36,39 Yunker et al.
suggests that ratios between 0.4 and 0.5 indicate liquid fossil
fuel combustion.35 Anthracene/(anthracene+phenanthrene)
ratios <0.1 indicate petrogenic sources and ratios >0.1 indicate
pyrogenic sources.35,39,40 A fifth ratio of two nonisomer parent
PAHs, benzo[a]pyrene/benzo[g,h,i]perylene, was used to
obtain sourcing information for the 5- and 6-ring PAHs
measured in this study. For this ratio, values >0.6 are indicative
of traffic emissions while values <0.6 indicate nontraffic
emission sources.39 There were samples in the middle and far
groups for which benzo[a]pyrene, benzo[g,h,i]perylene, or
both were below limits of detection (BLOD). So, the sample
sizes for the close, middle, and far groups for this final ratio are
5, 9, and 4, respectively.
Risk Assessment. The carcinogenic potency of the PAH
mixture at each site was calculated by multiplying the
concentration of each PAH by the relative potency factor
(RPF) it was given by the U.S. EPA.23 A list of the RPFs is in SI
Table S2. This estimate of carcinogenic potency is referred to
as the benzo[a]pyrene equivalent concentration, or BaPeq.

These values were used in quantitative risk assessments to
estimate cancer risks of exposure to the measured PAHs
through inhalation, using the EPA’s framework.41 Exposure
parameters were modeled after the “residential” and “outdoor
worker” examples presented to Superfund risk assessors by the
EPA in 2014.42 Specifically, the average lifetime was set at 70
years for all exposure scenarios. For the residential scenarios,
exposure duration and exposure frequency were set at 26 years
and 350 days/year, respectively. For the outdoor worker
scenario, these parameters were set at 25 years and 225 days/
year. The residential assessment was performed for a worst-case
and best-case scenario, by adjusting the daily exposure time to
24 or 1 h, while the outdoor worker assessment was performed
with daily exposure time set at 8 h. Risk assessment equations
are included as SI equations S4−S5.
Statistical Analysis. Welch’s two sample t tests were
performed on the data for ∑PAH 62 , benzo[a]pyrene,
phenanthrene, pyrene, and carcinogenic potency, between
each pairwise combination of distance groups, using R version
2.15.3. It was assumed that variance between each two groups
was unequal. Results were deemed significantly different when
α <0.05. Exploratory principle components analysis is included
in SI Figure S1.
Quality Control. During passive sampler preparation, one
LDPE strip was hung in the room to account for potential
contamination during PRC infusion. In the field, sampling was
replicated at one site, n = 3. A trip blank was taken to each
sampling site to account for contamination during transport.
One blank LDPE strip was included each day in the cleaning
process after deployment, as a cleaning blank. This also
doubled as a blank during sampler extraction. Perylene-d12 was
spiked into all extracts at 500 ng/mL before instrumental
analysis, to act as an internal standard. The analytical method
was validated using its calibration, precision and accuracy, and
detection limits prior to use. During instrument analysis,
instrument blanks and continuing calibration verifications were
run at the beginning and end of each set of samples. All
laboratory and field procedures were performed according to
FSES Standard Operating Procedures.

■

RESULTS AND DISCUSSION
PAH Levels and Trends. The data show a common trend:
PAH levels decrease as samplers get farther from active NGE
wells. Three distance groups were created, with the “close”
group <0.1 mile from an active well, the “middle” group
between 0.1 and 1.0 mile from an active well, and the “far”
group >1.0 mile from an active well. This trend is consistent
when comparing averages in the three distance groups for
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Figure 2. Average sum of 14 PAHs, grouped by distance to the closest active natural gas well, with comparisons to previous studies.29,44−46 All data
are vapor phase PAHs. The three distance groups in the present study are close (n = 5), middle (n = 12), and far (n = 6), defined in the text. Error
bars represent one SD.

Figure 3. Petrogenic vs. pyrogenic sourcing ratios, grouped by distance to the closest active natural gas well. a. Fluoranthene/pyrene, b.
phenanthrene/anthracene, c. fluoranthene/(fluoranthene+pyrene), and d. anthracene/(anthracene+phenanthrene) ratios. Pyrogenic and petrogenic
thresholds are defined in text. The three distance groups are close (n = 5), middle (n = 12), and far (n = 6), defined in the text. Error bars represent
one SD.

∑PAH62, benzo[a]pyrene, and phenanthrene (Figure 1a−c).
Average ∑PAH62 were 390, 300, and 270 ng/m3 for the close,
middle, and far groups. Phenanthrene was the most abundant
PAH in all samples, contributing over 30% to average ∑PAH62
in all distance groups. The next most abundant PAHs were

fluorene, pyrene, and fluoranthene, collectively contributing
more than an additional 35% to average ∑PAH62 in all distance
groups. The other 58 PAHs made up the remaining ∼30%.
The predominant health concerns associated with exposure
to PAH mixtures are cancer and respiratory distress, so
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pyrogenic signatures as samplers moved farther from NGE
activity (Figure 3a,c). Fluoranthene/(fluoranthene + pyrene)
ratios between 0.4 and 0.5 are associated with liquid fossil fuel
combustion.35 This may suggest that PAH source becomes
more affected by combustion as the sampler moves farther from
active wells. Exploratory principle components analysis
indicated that pyrene levels were negatively correlated with
distance to the closest active well, reinforcing the sourcing ratio
results (SI Figure S1). Additionally, average pyrene levels were
significantly higher in the close group than the far group,
reinforcing the association between NGE activity and pyrene
(Welch’s two sample t test, p < 0.05).
Average values for benzo[a]pyrene/benzo[g,h,i]perylene in
the close, middle and far groups were 0.88, 1.1, and 1.2. Given
that values >0.6 suggest traffic emissions, these data suggest
that higher molecular weight PAHs (≥5 rings) measured in this
study may be influenced by traffic emissions at all sites.
However, these 5- and 6- ring PAHs only contribute 3.4% on
average to ∑PAH across all sites.
The predominant petrogenic signature suggests that PAH
mixtures are heavily influenced by direct releases of hydrocarbons from NGE wells into the air, as opposed to other
myriad anthropogenic processes which would produce
pyrogenic signatures. It is reasonable to expect PAH emissions
alongside natural gas extraction. This association was
substantiated by a hydraulic fracturing simulation study,
which demonstrated that nonmethane hydrocarbons, including
aromatics, are emitted during natural gas extraction from
shale.47 Additionally, roughly half of the active wells were in the
producing phase during the sampling period. This may further
explain the predominant petrogenic signature, with PAHs
mixtures being heavily influenced by direct release of
hydrocarbons into the air, potentially as fugitive emissions
during production. This may also partially explain the higher
PAH load seen in the present study than in a previous study in
which PAHs were only sampled during the drilling phase.15
The petrogenic signature of measured PAHs and the increased
levels closer to NGE wells suggest that NGE activity may be
impacting ambient PAH levels in this rural area.
Wood burning is another common source of PAHs in air.
Retene is a PAH that is commonly used as an indicator of
biomass combustion, especially wood.48,49 Interestingly, average
retene levels did not show the same trend as other individual
PAHs across distance groups. Rather, average retene levels were
comparable across distance groups. This suggests that wood
burning had a similar impact on PAH levels in all distance
groups, and adds weight to the conclusion that elevated PAH
levels may be related to NGE activity, not to wood burning.
Carcinogenic Potency. Carcinogenic potency of PAH
mixtures decreases significantly in the far group, compared to
the close group (Welch’s two-sample t test, p < 0.05) (Figure
4). The average BaPeq concentrations in the close, middle and
far groups were 9.2, 8.0, and 6.3 ng/m3. Benzo[a]pyrene,
fluoranthene, and benzo[b]fluoranthene were the main
contributors to carcinogenic potency, collectively contributing
over 80% to the total potency in all groups. Specific
contributions to the average BaPeq in the close, middle and
far groups were as follows: benzo[b]fluoranthene contributed
2.2, 2.2, and 2.0 ng/m3, while fluoranthene contributed 2.4, 1.5,
and 1.4 ng/m3. Benzo[a]pyrene’s contributions were the same
as are listed above in relation to Figure 1, because benzo[a]pyrene has a relative potency factor of 1.

benzo[a]pyrene and phenanthrene were chosen as representative individual PAHs generally associated with each of these
health endpoints. Benzo[a]pyrene has been extensively studied
in relation to its carcinogenicity and phenanthrene has been
associated with respiratory distress.23,43 Average benzo[a]pyrene levels were 2.8, 2.7, and 1.9 ng/m3 for the close, middle,
and far groups. Average phenanthrene levels were 130, 96, and
88 ng/m3 for the close, middle, and far groups. The close and
far distance groups for benzo[a]pyrene were significantly
different (Welch’s two sample t test, p < 0.05). The close
and far distance groups for ∑PAH62 and phenanthrene were
just above the α = 0.05 significance level (Welch’s two sample t
tests, p = 0.053, and p = 0.061, respectively). Close and middle
groups for phenanthrene were also just above this significance
level (Welch’s two sample t test, p = 0.058).
Comparison to Literature Values. Results from the
present study were directly compared to the sum of 14 PAHs in
the air, reported in four previous studies (Figure 2). These 14
PAHs are listed in the SI. Average ∑PAH14 for the present
study were 330, 240, and 210 ng/m3 for the close, middle, and
far groups. Simcik et al. measured an average of 122 ng/m3
∑PAH20 in downtown Chicago, and an average of 21 ng/m3 in
a rural location in Michigan.44 Ravindra et al. measured average
∑PAH14 levels of 90 ng/m3 near a petroleum refinery in an
industrial Belgian location, and 9.4 ng/m3 in a rural Belgian
location.45 Khairy et al. used LDPE passive samplers to measure
an average ∑PAH14 of 110 ng/m3 in urban areas of Alexandria,
Egypt during winter sampling campaigns.29 Tidwell et al. used
LDPE passive samplers to measure PAHs on the shore during
the Deepwater Horizon Incident in the U.S. Gulf of Mexico. At
the two shoreline sites closest to the incident (Louisiana and
Mississippi), average ∑PAH14 were 6.3 ng/m3 in observations
immediately following the incident and 3.7 ng/m3 in all
subsequent observations over the following year.46 All of these
studies measured PAHs in the vapor phase, making results
comparable. Simcik and Ravindra et al. used active sampling to
measure vapor phase PAHs, while Khairy and Tidwell et al.
used LDPE passive sampling to measure PAHs in the vapor
phase. Thus, results from these previous studies are directly
comparable to the current work.
Thus, ∑PAH in the present study are higher or comparable
to most reported in published literature. Additionally,∑PAH in
the close group are roughly an order of magnitude greater than
levels previously measured in rural areas. The high density of
NGE wells in the study area is important when interpreting
these elevated PAH levels. Carroll County has more than 1 well
per square mile. So, even samples in the far group have
numerous active wells within 2 or 3 miles. This may partially
explain why PAH levels at all sites are elevated.
PAH Sourcing Techniques. Sourcing ratios indicate that
measured PAH mixtures have predominantly petrogenic
signatures (Figure 3a-d). Petrogenic signatures suggest that
PAHs were released directly from the earth, while pyrogenic
signatures suggest that PAHs came from combustion. For both
fluoranthene/pyrene and phenanthrene/anthracene, average
ratios were petrogenic for all distance groups (Figure 3a, b).
Fluoranthene/(fluoranthene+pyrene) ratios were petrogenic in
the close group, and gained more pyrogenic influence as
samples moved farther from NGE activity (Figure 3c).
Anthracene/(anthracene+phenanthrene) ratios were all petrogenic (Figure 3d). Fluoranthene/pyrene and fluoranthene/
(fluoranthene+pyrene) ratios both indicated that PAHs moved
from strongly petrogenic toward more mixed or slightly
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cancer risk, and this risk increases as exposure moves closer to
an active NGE well.
Quality Control Results. Carcinogenic PAHs were BLOD
in all quality control (QC) samples. Of the noncarcinogenic
PAHs, any instrument concentrations above the LODs in QC
samples translated to <2.0 ng/m3 in air, on average. Any
measurable levels in QC samples were averaged and subtracted
from sample concentrations. Including field and laboratory
blanks, >40% of analyzed samples were QC. PAH concentrations from the three codeployed samplers at the replicate site
were averaged, with an average standard deviation of 0.77 ng/
m3. Recoveries of laboratory surrogates ranged from 44 to 94%,
averaging 76%. Instrument concentrations were surrogatecorrected. Instrument blanks were BLOD for all PAHs.
Compounds were verified at ±20% of the true value for
>80% of PAHs using verified standards before instrumental
analyses of samples proceeded.
Additional Considerations. The LDPE passive samplers
used in this study sample the vapor phase, but the particulate
phase is typically enriched in carcinogenic PAHs. This is
because the majority of carcinogenic PAHs are higher
molecular weight, and the vapor phase typically contains a
larger fraction of low molecular weight PAHs, while the
particulate phase is typically enriched in high molecular weight
PAHs.53,54 This may mean that the potency values and risk
estimates presented here are under-representative of the actual
carcinogenic risk associated with the air in the study area.
Sampling sites were on the private property of volunteer
landowners. As a result, data do not represent a completely
random sample of the population, and statistical inferences are
only relevant to the portion of the population that was sampled.
As with any rapidly advancing technology, there are
differences in the techniques used to perform NGE in different
parts of the country and the world. It is possible that these
differences could impact PAH emissions, and thus that these
results may not be directly applicable to other regions. It has
been observed, for instance, that NGE activities in different
regions of the same state can have markedly different risks of
leaks.55 A recent commentary suggested that reasons for such
differences may include differing geology, rates of development,
techniques or implementation.56 All of these areas would be
worth exploring in efforts to minimize emissions from NGE in
the future.

Figure 4. Average carcinogenic potency of measured PAHs, grouped
by distance to the closest active natural gas well. The three distance
groups are close (n = 5), middle (n = 12), and far (n = 6), defined in
the text. Error bars represent one SD. The asterisk indicates a
significant difference between the close and far groups, p < 0.05.

Average BaPeq concentrations in all distance groups would
potentially be concerning as chronic doses. While there are
currently no regulatory levels for ambient PAH exposure in the
U.S., the U.S. Clean Air Act specifies that a pollutant can be
regulated when it is estimated to lead to more than 1 in a
million excess cancers over the lifetimes of the most exposed
individuals.50 The World Health Organization suggested that
0.012 ng/m3 BaP in ambient air would produce 1 excess cancer
in a million exposed individuals.51 Additionally, Caldwell et al.
proposed 0.48 ng/m3 BaP as the benchmark concentration
expected to cause excess cancer risk above 1 in a million.50 Both
WHO and the European Union have suggested 1.0 ng/m3 BaP
as a guidance level for ambient air concentrations.24,52 If this
guidance level were applied, ambient BaPeq at all sites in this
study would exceed this level.
Quantitative Risk Assessment. Quantitative risk assessment indicates that carcinogenic risk associated with inhalation
decreases as samplers move farther from active wells. For the
maximum residential exposure scenario of 24 h/day, estimated
excess lifetime cancer risk (ELCR) decreases from 290 to 200
in a million when moving from the close to far group. For the
minimum residential exposure scenario of 1 h/day, estimated
ELCR decreases from 12 to 8.1 in a million when moving from
the close to far group. The outdoor worker scenario was also
calculated to approximate exposures working outside amidst
NGE activity, such as farming or working on NGE wells. For
this scenario, estimated ELCR decreases from 59 to 40 in a
million when moving from the close to far group. These
estimations depend heavily on exposure time, exposure
frequency, and proximity to an active NGE well.
In all scenarios, the estimated ELCR decreases by about 30%
when moving from the close group to far group, all other
factors held constant. All of the estimated ELCRs were above 1
in a million, which is the conservative end of the range that the
U.S. EPA considers acceptable. The estimated ELCRs for the
maximum residential exposure convert to 2.9 in 10 000 and 2.0
in 10 000 for the close and far groups, respectively. These
values exceed 1 in 10 000, which is the least conservative end of
the U.S. EPA’s acceptable range. This suggests that the
maximum exposure scenario would produce risk levels above
the U.S. EPA’s acceptable range. Thus, PAH mixtures in areas
heavily impacted by NGE may have higher than acceptable

■

ASSOCIATED CONTENT

S Supporting Information
*

Additional details about sampling sites, sampling methods,
analytical methods, and data analysis are included in the SI.
This material is available free of charge via the Internet at
http://pubs.acs.org.

■

AUTHOR INFORMATION

Corresponding Author

*Phone: 541-737-8501; e-mail: kim.anderson@oregonstate.
edu.
Notes

The authors declare no competing financial interest.

■

ACKNOWLEDGMENTS
This work was funded by the National Institute of Environmental Health Sciences grants to Oregon State University: P30ES000210 and to the University of Cincinnati: P30-ES06096.
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to natural gas development in rural Colorado. Environ. Health. Perspect.
2014, 122 (4), 412−417.
(12) Roy, A. A.; Adams, P. J.; Robinson, A. L. Air pollutant emissions
from the development, production, and processing of Marcellus Shale
natural gas. J. Air Waste Manage. Assoc. 2014, 64 (1), 19−37.
(13) Litovitz, A.; Curtright, A.; Abramzon, S.; Burger, N.; Samaras, C.
Estimation of regional air-quality damages from Marcellus Shale
natural gas extraction in Pennsylvania. Environ. Res. Lett. 2013, 8 (1),
014017.
(14) Bunch, A.; Perry, C.; Abraham, L.; Wikoff, D.; Tachovsky, J.;
Hixon, J.; Urban, J.; Harris, M.; Haws, L. Evaluation of impact of shale
gas operations in the Barnett Shale region on volatile organic
compounds in air and potential human health risks. Sci. Total Environ.
2014, 468, 832−842.
(15) Colborn, T.; Schultz, K.; Herrick, L.; Kwiatkowski, C. An
Exploratory Study of Air Quality Near Natural Gas Operations. Hum.
Ecol. Risk Assess. 2014, 20 (1), 86−105.
(16) Rafferty, M. A.; Limonik, E. Is shale gas drilling an energy
solution or public health crisis? Public Health Nurs. 2013, 30 (5), 454−
462.
(17) Goldstein, B. D.; Brooks, B. W.; Cohen, S. D.; Gates, A. E.;
Honeycutt, M. E.; Morris, J. B.; Penning, T. M.; Orme-Zavaleta, J.;
Snawder, J. The role of toxicological science in meeting the challenges
and opportunities of hydraulic fracturing. Toxicol. Sci. 2014, 139 (2),
271−283.
(18) Fry, M. Urban gas drilling and distance ordinances in the Texas
Barnett Shale. Energy Policy 2013, 62, 79−89.
(19) Brasier, K. J.; Filteau, M. R.; McLaughlin, D. K.; Jacquet, J.;
Stedman, R. C.; Kelsey, T. W.; Goetz, S. J. Residents’ perceptions of
community and environmental impacts from development of natural
gas in the Marcellus Shale: A comparison of Pennsylvania and New
York cases. J. Rural Soc. Sci. 2011, 26 (1), 32−61.
(20) Rabinowitz, P. M.; Slizovskiy, I. B.; Lamers, V.; Trufan, S. J.;
Holford, T. R.; Dziura, J. D.; Peduzzi, P. N.; Kane, M. J.; Reif, J. S.;
Weiss, T. R. Proximity to natural gas wells and reported health status:
Results of a household survey in Washington County, Pennsylvania.
Environ. Health. Perspect. 2015, 123 (1), 21−26.
(21) U.S. EPA. Guidelines for Carcinogen Risk Assessment; Washington,
D.C., 2005.
(22) Macey, G.; Breech, R.; Chernaik, M.; Cox, C.; Larson, D.;
Thomas, D.; Carpenter, D. Air concentrations of volatile compounds
near oil and gas production: A community-based exploratory study.
Environ. Health 2014, 13 (82), 1−18.
(23) U.S. EPA. Development of a Relative Potency Factor (RPF)
Approach for Polycyclic Aromatic Hydrocarbon (PAH) Mixtures;
Intregrated Risk Information Systems (IRIS): Washington, D.C., 2010.
(24) Ravindra, K.; Sokhi, R.; Van Grieken, R. Atmospheric polycyclic
aromatic hydrocarbons: Source attribution, emission factors and
regulation. Atmos. Environ. 2008, 42 (13), 2895−2921.
(25) Perera, F. P.; Li, Z.; Whyatt, R.; Hoepner, L.; Wang, S.;
Camann, D.; Rauh, V. Prenatal airborne polycyclic aromatic
hydrocarbon exposure and child IQ at age 5 years. Pediatrics 2009,
124 (2), e195−e202.
(26) Petty, J. D.; Huckins, J. N.; Zajicek, J. L. Application of
semipermeable membrane devices (SPMDs) as passive air samplers.
Chemosphere 1993, 27 (9), 1609−1624.
(27) Prest, H. F.; Huckins, J. N.; Petty, J. D.; Herve, S.; Paasivirta, J.;
Heinonen, P. A survey of recent results in passive sampling of water
and air by semipermeable membrane devices. Mar. Pollut. Bull. 1995,
31 (4), 306−312.
(28) Bartkow, M. E.; Hawker, D. W.; Kennedy, K. E.; Müller, J. F.
Characterizing uptake kinetics of PAHs from the air using polyethylene-based passive air samplers of multiple surface area-to-volume
ratios. Environ. Sci. Technol. 2004, 38 (9), 2701−2706.
(29) Khairy, M. A.; Lohmann, R. Field validation of polyethylene
passive air samplers for parent and alkylated PAHs in Alexandria,
Egypt. Environ. Sci. Technol. 2012, 46 (7), 3990−3998.
(30) U.S. EIA. Oil and Natural Gas Drilling in Ohio on the Rise;
Energy Information Administration, U.S. Department of Energy, 2011.

We thank Glenn Wilson, Ricky Scott, Jorge Padilla, Gary
Points, and Melissa McCartney of the OSU FSES Program for
help with analysis. Thank you to Dr. Diana Rohlman of the
OSU Environmental Health Sciences Center Community
Outreach and Engagement Core (COEC), Sarah Elam of the
University of Cincinnati (UC) Environmental Health Sciences
Center COEC, Jody Alden of UC, and Paul Feezel of Carroll
Concerned Citizens, all for assistance with volunteer recruitment and communication. Thank you to Pierce Kuhnell of UC
for mapping sample sites. Finally, thank you to the volunteer
participants in Ohio for making this study possible.

■

ABBREVIATIONS
PAH polycyclic aromatic hydrocarbon
NGE natural gas extraction
VOC volatile organic compound
BTEX benzene toluene ethylbenzene xylenes
NOx nitrogen oxides
LDPE low-density polyethylene
OSU Oregon State University
FSES Food Safety and Environmental Stewardship
PRC performance reference compound
LOD limit of detection
LOQ limit of quantitation
BLOD below limit of detection
BaPeq benzo[a]pyrene equivalent
ELCR excess lifetime cancer risk
QC
quality control

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REFERENCES

(1) U.S. EIA. Annual Energy Outlook 2011 with Projections to 2035;
Energy Information Administration, U.S. Department of Energy, 2011.
(2) U.S. EIA. Review of Emerging Resources: US Shale Gas and Shale
Oil Plays; Energy Information Administration, U.S. Department of
Energy 2011.
(3) U.S. Congress. Energy Policy Act of 2005 In Public Law 109 -58,
2005.
(4) Centner, T. J.; O’Connell, L. K. Unfinished business in the
regulation of shale gas production in the United States. Sci. Total
Environ. 2014, 476, 359−367.
(5) Carlton, A. G.; Little, E.; Moeller, M.; Odoyo, S.; Shepson, P. B.
The data gap: Can a lack of monitors obscure loss of clean air act
benefits in fracking areas? Environ. Sci. Technol. 2014, 48, 893−894.
(6) Small, M. J.; Stern, P. C.; Bomberg, E.; Christopherson, S. M.;
Goldstein, B. D.; Israel, A. L.; Jackson, R. B.; Krupnick, A.; Mauter, M.
S.; Nash, J.; North, D. W.; Olmstead, S. M.; Prakash, A.; Rabe, B.;
Richardson, N.; Tierney, S.; Webler, T.; Wong-Parodi, G.; Zielinska, B.
Risks and risk governance in unconventional shale gas development.
Environ. Sci. Technol. 2014, 48, 8289−8297.
(7) Colborn, T.; Kwiatkowski, C.; Schultz, K.; Bachran, M. Natural
Gas Operations from a Public Health Perspective. Hum. Ecol. Risk
Assess. 2011, 17 (5), 1039−1056.
(8) Adgate, J. L.; Goldstein, B. D.; McKenzie, L. M. Potential public
health hazards, exposures and health effects from unconventional
natural gas development. Environ. Sci. Technol. 2014, 48 (15), 8307−
8320.
(9) Shonkoff, S. B.; Hays, J.; Finkel, M. L. Environmental public
health dimensions of shale and tight gas development. Environ. Health.
Perspect. 2014, 122 (8), 787−795.
(10) McKenzie, L. M.; Witter, R. Z.; Newman, L. S.; Adgate, J. L.
Human health risk assessment of air emissions from development of
unconventional natural gas resources. Sci. Total Environ. 2012, 424,
79−87.
(11) McKenzie, L. M.; Guo, R.; Witter, R. Z.; Savitz, D. A.; Newman,
L. S.; Adgate, J. L. Birth outcomes and maternal residential proximity
5209

DOI: 10.1021/es506095e
Environ. Sci. Technol. 2015, 49, 5203−5210

 Article

Environmental Science & Technology
(31) Ohio DNR. Utica/Point Pleasant Shale Wells; Division of Oil and
Gas Management, Ohio Department of Natural Resources, 2014.
(32) Anderson, K. A.; Sethajintanin, D.; Sower, G.; Quarles, L. Field
trial and modeling of uptake rates of in situ lipid-free polyethylene
membrane passive sampler. Environ. Sci. Technol. 2008, 42, 4486−
4493.
(33) Huckins, J. N., Petty, J. D., Booij, K. Monitors of Organic
Chemicals in the Environment; Springer: New York, 2006.
(34) Budzinski, H.; Jones, I.; Bellocq, J.; Pierard, C.; Garrigues, P.
Evaluation of sediment contamination by polycyclic aromatic hydrocarbons in the Gironde estuary. Mar. Chem. 1997, 58 (1), 85−97.
(35) Yunker, M. B.; Macdonald, R. W.; Vingarzan, R.; Mitchell, R.
H.; Goyette, D.; Sylvestre, S. PAHs in the Fraser River basin: A critical
appraisal of PAH ratios as indicators of PAH source and composition.
Org. Geochem. 2002, 33 (4), 489−515.
(36) Zhang, W.; Zhang, S.; Wan, C.; Yue, D.; Ye, Y.; Wang, X. Source
diagnostics of polycyclic aromatic hydrocarbons in urban road runoff,
dust, rain and canopy throughfall. Environ. Pollut. 2008, 153 (3), 594−
601.
(37) Fabbri, D.; Vassura, I.; Sun, C.-G.; Snape, C. E.; McRae, C.;
Fallick, A. E. Source apportionment of polycyclic aromatic hydrocarbons in a coastal lagoon by molecular and isotopic characterisation.
Mar. Chem. 2003, 84 (1), 123−135.
(38) Wang, Z.; Fingas, M.; Shu, Y.; Sigouin, L.; Landriault, M.;
Lambert, P.; Turpin, R.; Campagna, P.; Mullin, J. Quantitative
characterization of PAHs in burn residue and soot samples and
differentiation of pyrogenic PAHs from petrogenic PAHs-the 1994
mobile burn study. Environ. Sci. Technol. 1999, 33 (18), 3100−3109.
(39) Tobiszewski, M.; Namieśnik, J. PAH diagnostic ratios for the
identification of pollution emission sources. Environ. Pollut. 2012, 162,
110−119.
(40) Pies, C.; Hoffmann, B.; Petrowsky, J.; Yang, Y.; Ternes, T. A.;
Hofmann, T. Characterization and source identification of polycyclic
aromatic hydrocarbons (PAHs) in river bank soils. Chemosphere 2008,
72 (10), 1594−1601.
(41) U.S. EPA. Risk Assessment Guidance for Superfund; Office of
Superfund Remediation and Technology Innovation: Washington,
D.C., 2009.
(42) U.S. EPA. Memo: Recommended Default Exposure Factors; Office
of Solid Waste and Emergency Response: Washington, D.C., 2014.
(43) Tsien, A.; Diaz-Sanchez, D.; Ma, J.; Saxon, A. The organic
component of diesel exhaust particles and phenanthrene, a major
polyaromatic hydrocarbon constituent, enhances IgE production by
IgE-secreting EBV-transformed human B Cells in vitro. Toxicol. Appl.
Pharmacol. 1997, 142 (2), 256−263.
(44) Simcik, M. F.; Zhang, H.; Eisenreich, S. J.; Franz, T. P. Urban
contamination of the Chicago/Coastal Lake Michigan atmosphere by
PCBs and PAHs during AEOLOS. Environ. Sci. Technol. 1997, 31 (7),
2141−2147.
(45) Ravindra, K.; Bencs, L.; Wauters, E.; De Hoog, J.; Deutsch, F.;
Roekens, E.; Bleux, N.; Berghmans, P.; Van Grieken, R. Seasonal and
site-specific variation in vapour and aerosol phase PAHs over Flanders
(Belgium) and their relation with anthropogenic activities. Atmos.
Environ. 2006, 40 (4), 771−785.
(46) Tidwell, L. G.; Allan, S. E.; O’Connell, S.; Hobbie, K. A.; Smith,
B. W.; Anderson, K. A. PAH and OPAH air-water exchange during the
Deepwater Horizon oil spill. Environ. Sci. Technol. 2015, 49 (1), 141−
149.
(47) Sommariva, R.; Blake, R. S.; Cuss, R. J.; Cordell, R. L.;
Harrington, J. F.; White, I. R.; Monks, P. S. Observations of the release
of non-methane hydrocarbons from fractured shale. Environ. Sci.
Technol. 2014, 48 (15), 8891−8896.
(48) Ramdahl, T. Retenea molecular marker of wood combustion
in ambient air. Nature 1983, 306, 580−582.
(49) Shen, G.; Tao, S.; Wei, S.; Zhang, Y.; Wang, R.; Wang, B.; Li,
W.; Shen, H.; Huang, Y.; Yang, Y. Retene emission from residential
solid fuels in China and evaluation of retene as a unique marker for
soft wood combustion. Environ. Sci. Technol. 2012, 46 (8), 4666−4672.

(50) Caldwell, J. C.; Woodruff, T. J.; Morello-Frosch, R.; Axelrad, D.
A. Application of health information to hazardous air pollutants
modeled in EPA’s Cumulative Exposure Project. Toxicol. Ind. Health
1998, 14 (3), 429−454.
(51) WHO. Air Quality Guidelines for Europe; World Health
Organization Regional Office for Europe: Copenhagen, Denmark,
2000.
(52) EU. European Parliament legislative resolution on the proposal
for a European Parliament and Council directive on arsenic, cadmium,
mercury, nickel and polycyclic aromatic hydrocarbons in ambient air.
Off. J. Eur. Union 2004, C104E, 204−212.
(53) Hassan, S. K.; Khoder, M. I. Gas−particle concentration,
distribution, and health risk assessment of polycyclic aromatic
hydrocarbons at a traffic area of Giza, Egypt. Environ. Monit. Assess
2011, 184 (6), 3593−3612.
(54) Kameda, Y.; Shirai, J.; Komai, T.; Nakanishi, J.; Masunaga, S.
Atmospheric polycyclic aromatic hydrocarbons: Size distribution,
estimation of their risk and their depositions to the human respiratory
tract. Sci. Total Environ. 2005, 340 (1), 71−80.
(55) Ingraffea, A. R.; Wells, M. T.; Santoro, R. L.; Shonkoff, S. B.
Assessment and risk analysis of casing and cement impairment in oil
and gas wells in Pennsylvania, 2000−2012. Proc. Natl. Acad. Sci. 2014,
111 (30), 10955−10960.
(56) Jackson, R. B. The integrity of oil and gas wells. Proc. Natl. Acad.
Sci. 2014, 111 (30), 10902−10903.

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Environ. Sci. Technol. 2015, 49, 5203−5210