1,712
Views
0
CrossRef citations to date
0
Altmetric
Research Articles

Exposure to a mixture of 23 chemicals associated with unconventional oil and gas operations alters immune response to challenge in adult mice

, , , , &
Pages 105-117 | Received 13 Apr 2021, Accepted 04 Aug 2021, Published online: 28 Aug 2021

References

  • Bahadar H, Mostafalou S, Abdollahi M. 2014. Current understandings and perspectives on non-cancer health effects of benzene: A global concern. Toxicol Appl Pharmacol. 276(2):83–94.
  • Baines C, McKeown-Eyssen G, Riley N, Cole D, Marshall L, Loescher B, Jazmaji V. 2004. Case-control study of multiple chemical sensitivity, comparing hematology, biochemistry, vitamins and serum volatile organic compound measures. Occup. Med. 54(6):408–418.
  • Barrett T. 1985. Growth, purification and titration of influenza viruses. In: Mahy B, editors. Virology: A practical approach. Washington (DC): IRL Press. p. 119–150.
  • Bauer S, Roy A, Emo J, Chapman T, Georas S, Lawrence BP. 2012. The effects of maternal exposure to bisphenol A on allergic lung inflammation into adulthood. Toxicol Sci. 130(1):82–93.
  • Bolden A, Kwiatkowski C, Colborn T. 2015. New look at BTEX: Are ambient levels a problem? Environ Sci Technol. 49(9):5261–5276.
  • Boule L, Chapman T, Hillman S, Kassotis C, O'Dell C, Robert J, Georas S, Nagel S, Lawrence BP. 2018. Developmental exposure to a mixture of 23 chemicals associated with unconventional oil and gas operations alters the immune system of mice. Toxicol Sci. 163(2):639–654.
  • Boule L, Winans B, Lawrence BP. 2014. Effects of developmental activation of the AhR on CD4+ T-cell responses to influenza virus infection in adult mice. Environ Health Perspect. 122(11):1201–1208.
  • Brann E, Edvinsson A, Rostedt Punga A, Sundstrom-Poromaa I, Skalkidou A. 2019. Inflammatory and anti-inflammatory markers in plasma: From late pregnancy to early post-partum. Sci. Rep. 9:1863.
  • Chapman T, Georas S. 2014. Regulatory tone and mucosal immunity in asthma. Int Immunopharmacol. 23(1):330–336.
  • Cozzarelli IM, Skalak KJ, Kent DB, Engle MA, Benthem A, Mumford AC, Haase K, Farag A, Harper D, Nagel SC, et al. 2017. Environmental signatures and effects of an oil and gas wastewater spill in the Williston Basin, North Dakota. Sci Total Environ. 579:1781–1793.
  • Deziel N, Brokovich E, Grotto I, Clark C, Barnett-Itzhaki Z, Broday D, Shay K. 2020. Unconventional oil and gas development and health outcomes: A scoping review of the epidemiological research. Environ Res. 182:109124.
  • DiGiulio D, Jackson R. 2016. Impact to underground sources of drinking water and domestic wells from production well stimulation and completion practices in the Pavillion, Wyoming, Field. Environ Sci Technol. 50(8):4524–4536.
  • Elliott E, Ma X, Leaderer B, McKay L, Pedersen C, Wang C, Gerber C, Wright T, Sumner A, Brennan M, et al. 2018. A community-based evaluation of proximity to unconventional oil and gas wells, drinking water contaminants, and health symptoms in Ohio. Environ Res. 167:550–557.
  • Elsner M, Hoelzer K. 2016. Quantitative survey and structural classification of hydraulic fracturing chemicals reported in unconventional gas production. Environ Sci Technol. 50(7):3290–3314.
  • Fink A, Engle K, Ursin R, Tang W, Klein S. 2018. Biological sex affects vaccine efficacy and protection against influenza in mice. Proc Natl Acad Sci USA. 115(49):12477–12482.
  • Fletcher J, Lalor S, Sweeney C, Tubridy N, Mills K. 2010. T cells in multiple sclerosis and experimental autoimmune encephalomyelitis. Clin Exp Immunol. 162(1):1–11.
  • Gabriel G, Arck P. 2014. Sex, immunity, and influenza. J Infect Dis. 209(suppl 3):S93–S99.
  • Gross S, Avens H, Banducci A, Sahmel J, Panko J, Tvermoes B. 2013. Analysis of BTEX groundwater concentrations from surface spills associated with hydraulic fracturing operations. J Air Waste Manag Assoc. 63(4):424–432.
  • Hirahara K, Nakayama T. 2016. CD4+ T-cells subsets in inflammatory diseases: Beyond the TH1/TH2 paradigm. Int Immunol. 28(4):163–171.
  • Jemielita T, Gerton G, Neidell M, Chillrud S, Yan B, Stute M, Howarth M, Saberi P, Fausti N, Penning T, et al. 2015. Unconventional gas and oil drilling is associated with increased hospital utilization rates. PLOS One. 10(7):e1031093.
  • Kassotis C, Bromfield J, Klemp K, Meng C, Wolfe A, Zoeller R, Balise V, Isiguzo C, Tillitt D, Nagel S. 2016. Adverse reproductive and developmental health outcomes following prenatal exposure to a hydraulic fracturing chemical mixture in female C57Bl/6 mice. Endocrinology. 157(9):3469–3481.
  • Kassotis C, Klemp K, Vu D, Lin C, Meng C, Besch-Williford C, Pinatti L, Zoeller R, Drobnis E, Balise V, et al. 2015. Endocrine-disrupting activity of hydraulic fracturing chemicals and adverse health outcomes after prenatal exposure in male mice. Endocrinology. 156(12):4458–4473.
  • Kassotis C, Tillitt D, Davis J, Hormann A, Nagel S. 2014. Estrogen and androgen receptor activities of hydraulic fracturing chemicals and surface and groundwater in a drilling-dense region. Endocrinology. 155(3):897–907.
  • Kawabata T, and White K Jr. 1990. Effects of naphthalene and naphthalene metabolites on the in vitro humoral immune response. J Toxicol Environ Health. 30(1):53–67.
  • Klein S, Flanagan K. 2016. Sex differences in immune responses. Nat Rev Immunol. 16(10):626–638.
  • Knowlden S, Hillman S, Chapman T, Patil R, Miller D, Tigyi G, Georas S. 2016. Novel inhibitory effect of a lysophosphatidic acid 2 agonist on allergen-driven airway inflammation. Am J Respir Cell Mol Biol. 54(3):402–409.
  • Langier S, Sade K, Kivity S. 2012. Regulatory T-cells in allergic asthma. Isr Med Assoc J. 14(3):180–183.
  • Lawrence BP, Roberts A, Neumiller J, Cundiff J, Woodland D. 2006. Aryl hydrocarbon receptor activation impairs the priming but not the recall of influenza virus-specific CD8+ T cells in the lung. J Immunol. 177(9):5819–5828.
  • Lawrence BP, Warren T, Luong H. 2000. Fewer T-lymphocytes and decreased pulmonary influenza virus burden in mice exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). J Toxicol Environ Health. 61:39–53.
  • Li H, Li D, He Z, Fan J, Li Q, Liu X, Guo P, Zhang H, Chen S, Li Q, et al. 2018. The effects of Nrf2 knockout on regulation of benzene-induced mouse hematotoxicity. Toxicol Appl Pharmacol. 358:56–67.
  • Lima J, Martins C, Leandro M, Nunes G, Sousa M, Branco J, Borrego L. 2016. Characterization of B-cells in healthy pregnant women from late pregnancy to post-partum: A prospective observational study. BMC Pregnancy Childbirth. 16(1):139.
  • Malaise Y, Lencina C, Cartier C, Olier M, Menard S, Guzylack-Piriou L. 2020. Perinatal oral exposure to low doses of bisphenol A, S, or F impairs immune functions at intestinal and systemic levels in female offspring mice. Environ Health. 19:93.
  • Maloney K, Baruch-Mordo S, Patterson L, Nicot J, Entrekin S, Fargione J, Kiesecker J, Konschnik K, Ryan J, Trainor A, et al. 2017. Unconventional oil and gas spills: Materials, volumes, and risks to surface waters in four states of the U.S. Sci Total Environ. 581–582:369–377.
  • Marina M. 2014. Xenoestrogens challenge 17β-estradiol protective effects in colon cancer. World J Gastrointest Oncol. 6(3):67–73.
  • Martins C, Lima J, Nunes G, Borrego L. 2017. Regulatory T- and B-cells in asthmatic women: variations from pregnancy to postpartum. J Investig Allergol Clin Immunol. 27(1):46–57.
  • McClelland E, Smith J. 2011. Gender specific differences in the immune response to infection. Arch Immunol Ther Exp. 59(3):203–213.
  • McGuire C, Lawrence BP, Robert J. 2021. Thyroid disrupting chemicals in mixture perturb thymocyte differentiation in Xenopus laevis tadpoles. Toxicol Sci. 166(1):39–50.
  • McHale C, Zhang L, Smith M. 2012. Current understanding of the mechanism of benzene-induced leukemia in humans: Implications for risk assessment. Carcinogenesis. 33(2):240–252.
  • McKenzie L, Allshouse W, Byers T, Bedrick E, Serdar B, Adgate J. 2017. Childhood hematologic cancer and residential proximity to oil and gas development. PLOS One. 12(2):e0170423.
  • McKenzie L, Guo R, Witter R, Savitz D, Newman L, Adgate J. 2014. Birth outcomes and maternal residential proximity to natural gas development in rural Colorado. Environ Health Perspect. 122(4):412–417.
  • Mendel I, Kerlero de Rosbo N, Ben-Nun A. 1995. A myelin oligodendrocyte glycoprotein peptide induces typical chronic experimental autoimmune encephalomyelitis in H-2b mice: Fine specificity and T-cell receptor V β expression of encephalitogenic T-cells. Eur J Immunol. 25(7):1951–1959.
  • Nagel S, Kassotis C, Vandenberg L, Lawrence BP, Robert J, Balise V. 2020. Developmental exposure to a mixture of unconventional oil and gas chemicals: A review of experimental effects on adult health, behavior, and disease. Mol Cell Endocrinol. 513:110722.
  • Ngo S, Steyn F, McCombe P. 2014. Gender differences in autoimmune disease. Front Neuroendocrinol. 35(3):347–369.
  • Oertelt-Prigione S. 2012. The influence of sex and gender on the immune response. Autoimmun Rev. 11(6–7):A479–485.
  • Orem W, Varonka M, Crosby L, Haase K, Loftin K, Hladik M, Akob DM, Tatu C, Mumford A, Jaeschke J, et al. 2017. Organic geochemistry and toxicology of a stream impacted by unconventional oil and gas wastewater disposal operations. Appl Geochem. 80:155–167.
  • Peckham H, de Gruijter N, Raine C, Radziszewska A, Ciurtin C, Wedderburn L, Rosser E, Webb K, Deakin C. 2020. Male sex identified by global COVID-19 meta-analysis as a risk factor for death and ITU admission. Nat Commun. 11(1):6317.
  • Rabinowitz P, Slizovskiy I, Lamers V, Trufan S, Holford T, Dziura J, Peduzzi P, Kane M, Reif J, Weiss T, et al. 2015. Proximity to natural gas wells and reported health status: Results of a household survey in Washington County, Pennsylvania. Environ Health Perspect. 123(1):21–26.
  • Rasmussen S, Ogburn E, McCormack M, Casey J, Bandeen-Roche K, Mercer D, Schwartz B. 2016. Association between unconventional natural gas development in the Marcellus shale and asthma exacerbations. JAMA Intern Med. 176(9):1334–1343.
  • Reilly E, Martin K, Jin G, Yee M, O'Reilly M, Lawrence BP. 2015. Neonatal hyperoxia leads to persistent alterations in NK responses to influenza A virus infection. Am J Physiol Lung Cell Mol Physiol. 308(1):L76–85.
  • Robert J, McGuire C, Kim F, Nagel S, Price S, Lawrence BP, de J, Andino F. 2018. Water contaminants associated with unconventional oil and gas extraction cause immunotoxicity to amphibian tadpoles. Toxicol Sci. 166(1):39–50.
  • Robert J, McGuire C, Nagel S, Lawrence BP, Andino F. 2019. Developmental exposure to chemicals associated with unconventional oil and gas extraction alters immune homeostasis and viral immunity of the amphibian xenopus. Sci Total Environ. 671:644–654.
  • Robinson A, Harp C, Noronha A, Miller S. 2014. Experimental autoimmune encephalomyelitis (EAE) model of MS: Utility for understanding disease pathophysiology and treatment. Handb Clin Neurol. 122:173–189.
  • Stromnes I, Goverman J. 2006. Active induction of experimental allergic encephalomyelitis. Nat Protoc. 1(4):1810–1819.
  • Strutt T, McKinstry K, Marshall N, Vong A, Dutton R, Swain S. 2013. Multipronged CD4+ T-cells effector and memory responses cooperate to provide potent immunity against respiratory virus. Immunol Rev. 255(1):149–164.
  • Swain S, McKinstry K, Strutt T. 2012. Expanding roles for CD4+ T-cells in immunity to viruses. Nat Rev Immunol. 12(2):136–148.
  • Tsangari X, Andrianou XD, Agapiou A, Mochalski P, Makris KC. 2017. Spatial characteristics of urinary BTEX concentrations in the general population. Chemosphere. 173:261–266.
  • Tscharke D, Croft N, Doherty P, la Gruta N. 2015. Sizing up the key determinants of the CD8+ T-cell response. Nat Rev Immunol. 15(11):705–716.
  • Tustin A, Hirsch A, Rasmussen S, Casey J, Bandeen-Roche K, Schwartz B. 2017. Associations between unconventional natural gas development and nasal and sinus, migraine headache, and fatigue symptoms in Pennsylvania. Environ Health Perspect. 125(2):189–197.
  • United States Environmental Protection Agency (USEPA). 2021. Hydraulic fracturing for oil and gas: Impacts from the hydraulic fracturing water cycle on drinking water resources in the United States (final report). https://cfpub.epa.gov/ncea/hfstudy/recordisplay.cfm?deid=332990
  • Vengosh A, Jackson R, Warner N, Darrah T, Kondash A. 2014. A critical review of the risks to water resources from unconventional shale gas development and hydraulic fracturing in the United States. Environ Sci Technol. 48(15):8334–8348.
  • Veraldi A, Costantini A, Bolejack V, Miligi L, Vineis P, van Loveren H. 2006. Immunotoxic effects of chemicals: A matrix for occupational and environmental epidemiological studies. Am J Ind Med. 49(12):1046–1055.
  • Vorderstrasse B, Cundiff J, Lawrence BP. 2006. A dose-response study of the effects of prenatal and lactational exposure to TCDD on the immune response to influenza A virus. J Toxicol Environ Health A. 69(6):445–463.
  • Vroman H, van den Blink B, Kool M. 2015. Mode of dendritic cell activation: The decisive hand in TH2/TH17 cell differentiation. Implications in asthma severity? Immunobiology. 220(2):254–261.
  • Wang F, Liu F, Liu H, Chen W, Si X, Ma X. 2016. Effects of immunological and hematological parameter in mice exposed to mixture of volatile organic compounds. Inhal Toxicol. 28(4):164–169.
  • Webb E, Bushkin-Bedient S, Cheng A, Kassotis C, Balise V, Nagel S. 2014. Developmental and reproductive effects of chemicals associated with unconventional oil and natural gas operations. Rev Environ Health. 29:307–318.
  • Wen H, Yuan L, Wei C, Zhao Y, Qian Y, Ma P, Ding S, Yang X, Wang X. 2016. Effects of combined exposure to formaldehyde and benzene on immune cells in the blood and spleen in Balb/c mice. Environ Toxicol Pharmacol. 45:265–273.
  • World Health Organization (WHO). 2016. Protecting surface water for health. Geneva: World Health Organization Report.
  • Xie L, Gong W, Chen J, Xie H, Wang M, Yin X, Wu W. 2018. The flavonoid kurarinone inhibits clinical progression of EAE through inhibiting TH1 and TH17 cell differentiation and proliferation. Int Immunopharmacol. 62:227–236.
  • Yoshida Y, Liu J, Sugiura T, Ishidao T, Ueno S, Yanagita H, Fueta Y, Kunugita N, Hori H, Yamashita U, et al. 2009. The indoor air pollutant 2-ethyl-hexanol activates CD4 cells. Chem Biol Interact. 177(2):137–141.
  • Zabrodskii P, Kirichuk V, Osipov O. 2002. In vitro effects of alcohols and their metabolites on antibody-forming activity of T- and B-lymphocytes. Exp Biol Med. 133(3):258–260.