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Exploring the endocrine activity of air pollutants associated with unconventional oil and gas extraction

Fig. 1 Number of UOG air sampling studies by geologic formation. Air sampling has been performed in various UOG sites in the US. The most commonly sampled site in studies identified by our search was the Barnett Shale located in TX.

Abstract

Background

In the last decade unconventional oil and gas (UOG) extraction has rapidly proliferated throughout the United States (US) and the world. This occurred largely because of the development of directional drilling and hydraulic fracturing which allows access to fossil fuels from geologic formations that were previously not cost effective to pursue. This process is known to use greater than 1,000 chemicals such as solvents, surfactants, detergents, and biocides.

Authors:
Ashley L. Bolden, Kim Schultz, Katherine E. Pelch and Carol F. Kwiatkowski

1The Endocrine Disruption Exchange (TEDX), www.TEDX.org, Eckert, Colorado, USA

Received: 4 September 2017, Accepted: 20 February 2018, Published: 21 March 2018

In addition, a complex mixture of chemicals, including heavy metals, naturally-occurring radioactive chemicals, and organic compounds are released from the formations and can enter air and water. Compounds associated with UOG activity have been linked to adverse reproductive and developmental outcomes in humans and laboratory animal models, which is possibly due to the presence of endocrine active chemicals.

Methods

Using systematic methods, electronic searches of PubMed and Web of Science were conducted to identify studies that measured chemicals in air near sites of UOG activity. Records were screened by title and abstract, relevant articles then underwent full text review, and data were extracted from the studies. A list of chemicals detected near UOG sites was generated. Then, the potential endocrine activity of the most frequently detected chemicals was explored via searches of literature from PubMed.

Results

Evaluation of 48 studies that sampled air near sites of UOG activity identified 106 chemicals detected in two or more studies. Ethane, benzene and n-pentane were the top three most frequently detected. Twenty-one chemicals have been shown to have endocrine activity including estrogenic and androgenic activity and the ability to alter steroidogenesis. Literature also suggested that some of the air pollutants may affect reproduction, development, and neurophysiological function, all endpoints which can be modulated by hormones. These chemicals included aromatics (i.e., benzene, toluene, ethylbenzene, and xylene), several polycyclic aromatic hydrocarbons, and mercury.

Conclusion

These results provide a basis for prioritizing future primary studies regarding the endocrine disrupting properties of UOG air pollutants, including exposure research in wildlife and humans. Further, we recommend systematic reviews of the health impacts of exposure to specific chemicals, and comprehensive environmental sampling of a broader array of chemicals.

Background

Advanced techniques used to develop oil and gas resources, including horizontal drilling and hydraulic fracturing (fracking), have unlocked fossil fuels from formations previously unavailable for extraction, including shale and tight sands. Research has found that unconventional oil and gas (UOG) development and production is associated with air pollution [1, 2, 3, 4, 5, 6, 7], contamination of surface, ground, and drinking water [8, 9, 10], as well as soil and sediment contamination [11, 12, 13]. Contaminants released from UOG sites enter the air readily during well pad development and continue for the life of the well, impacting both local and regional air quality.

Industry wide there are hundreds of different products composed of a mixture of chemicals used during drilling, fracturing, and the cleaning and maintenance of well pads and equipment. Many of them are volatile and include several known carcinogens and hazardous air pollutants (HAPs) listed under the Clean Air Act [14]. Air pollutants are released both from the products and mobile and stationary equipment commonly used during UOG operations [6, 15, 16]. Further, unprocessed natural gas contains many volatile compounds that surface with methane and are released to the environment through venting and flaring and through fugitive emissions from well pipe fittings and equipment [6, 16, 17, 18].

Additionally, open evaporation pits that contain fracking fluids that return to the surface (flowback) and water produced from fracturing the formation (produced water) further impact air quality in these areas [19, 20, 21]. Due to the potential for wide-spread exposure to air pollutants released from UOG activity and the growing number of oil and gas wells being drilled in close proximity to neighborhoods, including schools and recreational areas, the health of nearby communities may be at risk. Indeed, several studies have shown that UOG activity may adversely impact the health of humans and animals [22, 23, 24, 25, 26] and the environment [27, 28, 29].

These concerns have led to a growth in epidemiologic research with many studies suggesting a link between UOG proximity and adverse health impacts. Self-reported symptoms by Pennsylvania residents living near UOG operations in the Marcellus Shale include impacts to the upper respiratory system, irritation of the skin and sensory organs, and increased headaches [25, 30]. Additional studies also considered well activity or density, a method used to estimate exposure to air pollutants. McKenzie et al., found an increased risk of neurological and respiratory effects, blood disorders, and adverse developmental outcomes in Colorado residents living within one-half mile of natural gas wells [31].

These observations were more pronounced during well completion activities [31]. Increased odds of asthma exacerbations [32], nasal irritation, migraine headaches, and fatigue symptoms were more often reported by residents living near sites with higher UOG activity compared to a control population [33]. Risk of childhood hematologic cancer was also increased with increased density of UOG wells [34]. Further, retrospective cohort studies have linked UOG activity to adverse reproductive and developmental outcomes, such as preterm birth [35, 36], low birth weight [37], congenital anomalies [38], and infant mortality [36, 39]. These outcomes suggest a possible relationship between maternal exposure to endocrine disrupting chemicals and birth outcomes; however, results across studies are mixed.

In addition to epidemiological studies, recent studies using in vitro and experimental animal models to assess the connection between UOG activity and endocrine-related outcomes have been published. In these initial studies chemicals detected in water collected near UOG operations such as spill sites and surface water near wastewater injection sites were shown to have activity in estrogen, androgen, progesterone, glucocorticoid, and thyroid hormone in vitro receptor assays [10, 40]. In laboratory experiments exposure has resulted in similar impacts across several different models.

Specifically, male rodents exposed prenatally to a mixture of chemicals used during hydraulic fracturing were shown to have increased organ weights of the testes and thymus, decreased sperm counts, and increased serum testosterone levels [41]. Effects in female rodents included hormone suppression, changes in uterine, ovary, heart, and body weights, and disrupted folliculogenesis [42]. Emerging research in zebrafish embryos found that exposure to flowback/produced water from UOG increased embryo deformations and mortality, reduced metabolic rates, and altered cardio-respiratory gene expression [43, 44].

Further, embryonically exposed juveniles demonstrated decreased metabolic rates and fitness as judged by swim performance [45]. In exposed juvenile rainbow trout mRNA expression was elevated for several genes including vitellogenin and estrogen receptor alpha 2. Additionally, expression of oxidative stress and biotranformation genes in the liver and gills was observed [46]. Finally, exposure of Daphnia to flowback/produced water resulted in decreased reproduction and altered gene expression [47].

The purpose of this evaluation was to employ systematic screening-level methods to begin to prioritize air pollutants associated with UOG that have evidence of endocrine activity. This work could be used to identify avenues for primary research to understand endocrine disrupting properties of air pollutants; provide the groundwork for in-depth reviews of the health impacts of exposure to specific chemicals (i.e., systematic or scoping reviews); offer rationale for further exposure research in wildlife and humans; and lastly, identify research gaps. Specifically, two objectives were completed; 1) identification of the most commonly detected chemicals in the air near UOG activity, as reported in original research, and 2) to determine if this subset of air pollutants has been shown to have endocrine activity or have effects that could be linked to disrupted endocrine signaling.

Methods

Identification of air pollutants near sites of UOG activity

Comprehensive literature searches were performed in order to identify studies that measured compounds in air near or on sites of UOG development in the United States (US). We used Web of Science and PubMed to complete electronic searches for all years to June 2016. The search logic was developed using terms for major geologic formations in the US where UOG activity occurs and terms that linked the formations to air emissions (Additional file 1: Table S1). The titles and abstracts of these articles were then screened for relevance using Distiller SR® [48] by two independent reviewers.

For inclusion, studies had to present primary findings, be in the English language, and measure air pollutants near sites of UOG production. Studies that only measured methane were excluded. Discrepancies regarding inclusion were discussed and resolved by the two reviewers. Summary level data from relevant studies were collected. Parameters included publication date, chemicals detected, and the location of measurement. These data were used to develop the list of compounds detected in air. This initial list was then used to yield a list of the chemicals detected in greater than 10 UOG air sampling studies.

Determination of endocrine activity of UOG related air pollutants

The list of air pollutants associated with UOG production ascertained from peer-reviewed literature was cross-referenced with the Endocrine Disruption Exchange (TEDX) List of Potential Endocrine Disruptors (http://endocrinedisruption.org/interactive-tools/tedx-list-of-potential-endocrine-disruptors/search-the-tedx-list: accessed October 2016) to determine if any of the chemicals had been characterized as having endocrine activity [49]. The TEDX List of Potential Endocrine Disruptors is a database that contains expert verified citations illustrating evidence of endocrine disruptive properties of a variety of chemicals; this database is continually updated as new evidence about chemicals becomes available [49].

Cross-referencing yielded the initial list of chemicals with evidence of endocrine activity. For this initial list, citations from the TEDX List of Potential Endocrine Disruptors were used as evidence of endocrine activity. We then performed searches in PubMed using the chemical name and CAS number for the remaining chemicals detected in greater than 10 UOG air sampling studies to determine whether or not those chemicals had evidence documented in the peer-reviewed literature regarding their potential endocrine activity (for the individual chemical search terms see Additional file 1: Table S2).

The following 15 chemicals were searched in PubMed: ethane, n-pentane, propane, n-butane, isopentane, isobutane, m,p-xylene, o-xylene, ethylene, methylcyclohexane, n-heptane, acetylene, n-octane, propylene, and cyclohexane. The PubMed records were imported into Sciome Workbench for Interactive computer-Facilitated Text-mining (SWIFT)-Review [50] and filtered using search terms (modified from [51, 52]) intended to identify articles that assessed the endocrine activity of the compounds (see Additional file 1: Table S3). Though xylenes (the isomeric mixture) is listed on the TEDX List of Potential Endocrine Disruptors we performed searches for the compounds as represented in the air sampling studies (i.e., m,p-xylene and o-xylene). In addition, studies that evaluated the effects of exposure to m-xylene and p-xylene separately and citations from the TEDX List of Potential Endocrine Disruptors that assessed the xylenes were included.

Results

Our search of the literature from PubMed and Web of Science yielded 1366 and 2907 potential records, respectively (including any duplicate records). Screening of titles and abstracts by two reviewers identified 97 relevant articles. Full text review of the articles yielded 43 inclusions and 54 exclusions (30 duplicates, five that did not assess specific chemicals, 10 reviews, four conference abstracts, and five categorized as other [e.g., methods development]). In addition, hand searching yielded five other studies that met inclusion criteria, resulting in a total of 48 included studies.

Table 1 lists the 48 citations of the articles that measured air pollutants on or near sites of UOG production. A distribution of the studies measuring UOG air pollutants in sites across the US is shown in Fig. 1. The majority of studies were done on the Barnett Shale in Texas (11 studies).

Table 1 List of citations for UOG air papers Table 1 List of citations for UOG air papers Table 1 List of citations for UOG air papers
Table 1 List of citations for UOG air papers

The least studied were Eagle Ford Shale in Texas, Haynesville Shale in Louisiana, Arkansas, and Texas, Fayetteville Shale in Arkansas, and Powder River Basin in Montana and Wyoming, all with only one study each. One hundred six chemicals were detected in two or more of the 48 studies that measured air pollutants near UOG sites and another 115 were detected only once (see Additional file 1: Table S4 for full list of detected chemicals). These chemicals represented a variety of classes including alkanes, alkenes, alkynes, aromatics, aldehydes and polycyclic aromatic hydrocarbons (PAHs). Twenty chemicals were detected in 10 or more studies with ethane and benzene being the most detected, appearing in 56% and 54% of studies, respectively. Fifty-four chemicals were detected in 3-9 studies and 147 were detected in 2 or fewer.

Fig. 1 Number of UOG air sampling studies by geologic formation. Air sampling has been performed in various UOG sites in the US. The most commonly sampled site in studies identified by our search was the Barnett Shale located in TX.
Fig. 1 Number of UOG air sampling studies by geologic formation. Air sampling has been performed in various UOG sites in the US. The most commonly sampled site in studies identified by our search was the Barnett Shale located in TX. The least frequently studied were Eagle Ford Shale, Fayetteville Shale, Haynesville Shale, and Powder River Basin. TX, Texas; AR, Arkansas; OK, Oklahoma; LA, Louisiana; MT, Montana; WY, Wyoming; NY, New York; MD, Maryland; PA, Pennsylvania; WV, West Virginia; OH, Ohio; VA, Virginia; KY, Kentucky; TN, Tennessee; CO, Colorado; ND, North Dakota; UT, Utah; KS, Kansas; NE, Nebraska; UOG, unconventional oil and gas

The list of chemicals detected near UOG activity was cross-referenced with the TEDX List of Potential Endocrine Disruptors. Twenty-six were already identified and listed in the TEDX List of Potential Endocrine Disruptors [49]. There were 15 additional chemicals that were reported as being detected in 10 or more UOG studies, but that were not currently included in the TEDX List of Potential Endocrine Disruptors that were searched.

A chemical’s absence on the TEDX List of Potential Endocrine Disruptors does not necessarily mean there is no evidence for endocrine activity. Rather, it is possible that the literature available for that chemical has not yet been investigated for endocrine activity. The searches of PubMed for the 15 frequently detected chemicals yielded eight with evidence from the literature indicating at least one study had shown the chemicals to be endocrine active (including findings related to potential endocrine activity).

Those chemicals were m-xylene, p-xylene, o-xylene, methylcyclohexane, n-heptane, isopentane, propane, propylene. There were no studies that evaluated the endocrine activity of ethane, n-butane, isobutane, ethylene, cyclohexane and acetylene found in our searches. In studies identified by our search that assessed the effects of n-pentane [53] and n-octane [54] endocrine activity was not shown. Table 2 characterizes possible endocrine activities for the individual chemicals. The studies listed in this table tested more direct indicators of endocrine activity such as estrogenic, androgenic, thyroidogenic, progestrogenic, glucocorticodogenic, and steroidogenic activities.

Table 2 Selected studies indicating endocrine activity*
Twenty-one air pollutants had evidence indicating that they impact hormone production, mimic hormones, or inhibit hormone signaling. There were 19 chemicals listed on the TEDX List of Potential Endocrine Disruptors and two that were identified via PubMed searches of frequently detected UOG air pollutants. The studies listed in the table tested estrogenic, androgenic, thyroidogenic, progestrogenic, glucocorticodogenic, and steroidogenic activity in various manners including: in vitro steroidogenesis, receptor mediated reporter gene activity, vitellogenin induction assays, and epidemiological, in vivo and ex vivo experimental animal assessments. ^hazardous air pollutant (HAP) * Note: all possible endocrine activities for the individual chemicals are not described.

Table 2 Selected studies indicating endocrine activity*

In Table 3, chemicals identified as having evidence of physiological activity that may be linked to endocrine disruption are shown. This includes evaluations of reproduction, aryl hydrocarbon signaling, development, neurophysiology, and other endocrine related effects. Notably, a few of these air pollutants (e.g., benzene, n-hexane, and isopentane) may impact less commonly evaluated endocrine related endpoints such as insulin signaling and adrenal physiology (see Table 3). Roughly half of the chemicals in Tables 2 and 3 are PAHs, although it should be noted that few studies detected PAHs near UOG (see Fig. 2).

Single ring aromatics such as benzene, toluene, ethylbenzene, xylene, and styrene are also shown in Tables 2 and 3 with evidence suggesting possible estrogenic, androgenic, reproductive, and developmental effects. Styrene seems to be of particular concern because in addition to the aforementioned evidence of endocrine activity it also appears to have evidence for glucocorticodogenic, thyroidogenic, and progestrogenic, activity and alterations of steroidgenesis.

Table 3 Selected studies demonstrating effects potentially related to endocrine disruption*
Thirty-three air pollutants had evidence indicating they impacted processes and systems that are modulated by endocrine signaling. There were 25 chemicals listed on the TEDX list of Potential endocrine disruptors and eight that were identified via PubMed searches of frequently detected UOG air pollutants. The studies listed in the table tested aryl hydrocarbon signaling, reproductive, developmental, neurophysiological, and other endocrine related effects in epidemiological, in vivo and ex vivo experimental animal assessments, in vitro embryonic culture and receptor mediated reporter gene activity assays. a insulin resistance; b adrenal physiology; c insulin binding; d hyperplasia of pituitary and thyroid; e retinoic acid signaling; ^hazardous air pollutant (HAP). * Note that all potentially related endocrine impacts for the individual chemicals are not described

Table 3 Selected studies demonstrating effects potentially related to endocrine disruption*

In Fig. 2, the air sampling data (Table 1) was combined with the data that assessed possible endocrine activity (Tables 2 and 3). The chemicals identified as potentially endocrine active are listed along with the number of studies that detected them in air near sites of UOG activity. This list included 34 chemicals with m-xylene and p-xylene counted separately, however they are combined (i.e., m,p-xylene) for the number of papers that detected them in the air to be consistent with how they are reported in that literature. In total, this list includes the 26 chemicals that were already on the TEDX List of Potential Endocrine Disruptors and the eight frequently detected UOG associated air pollutants that were found to have potential endocrine activity. Benzene, toluene, ethylbenzene, and xylenes (BTEX) were detected more frequently than PAHs and heavy metals such as mercury.

Fig. 2 Potentially endocrine active chemicals and the number of studies that identified them near UOG sites. The figure shows the 34 chemicals (with m-xylene and p-xylene counted separately) that were identified as having evidence of endocrine active properties and the number of times they were detected in the air sampling papers included in this study
Fig. 2 Potentially endocrine active chemicals and the number of studies that identified them near UOG sites. The figure shows the 34 chemicals (with m-xylene and p-xylene counted separately) that were identified as having evidence of endocrine active properties and the number of times they were detected in the air sampling papers included in this study. The graph show that the BTEX compounds (benzene, toluene, ethylbenzene, xylenes) were among the most frequently detected, and the polycyclic aromatic hydrocarbons (PAHs) were less frequently detected in air samples

Exploring the endocrine activity of air pollutants associated with unconventional oil and gas extraction

In the last decade unconventional oil and gas (UOG) extraction has rapidly proliferated throughout the United States (US) and the world. This occurred largely because of the development of directional drilling and hydraulic fracturing which allows access to fossil fuels from geologic formations that were previously not cost effective to pursue. This process is known to use greater than 1,000 chemicals such as solvents, surfactants, detergents, and biocides. In addition, a complex mixture of chemicals, including heavy metals, naturally-occurring radioactive chemicals, and organic compounds are released from the formations and can enter air and water.
Emanuel Martin
Emanuel Martin is a Petroleum Engineer graduate from the Faculty of Engineering and a musician educate in the Arts Faculty at National University of Cuyo. In an independent way he’s researching about shale gas & tight oil and building this website to spread the scientist knowledge of the shale industry.
http://www.allaboutshale.com

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