Abstract
Hydraulic fracturing (fracking) chemicals are used to maximize the extraction of hard-to-reach underground energy resources. Large amounts of fracking fluid could escape to the surrounding environments, including underground and surface water resources, during the chemical mixing stage of the hydraulic fracturing water cycle due to equipment failure or human error. However, the impact of pollution resulting from operational discharges is difficult to assess in aquatic ecosystems. In this study, pathological investigations, chromosomal aberrations, DNA damage, and biochemical and hematological parameters were used to evaluate the effects of such chemicals on Nile tilapia. Chromosomal aberrations are considered very sensitive genetic markers of exposure to genotoxic chemicals and are used as indicators of DNA damage. The appearance of different types of chromosomal aberrations (gaps and breaks) due to chemical exposure was significantly reduced by treatment with spirulina. Various deleterious findings in Nile tilapia, in the current study, could attributed to the presence of fracking chemicals in the aquatic environment. However, the presence of spirulina in the diet reduced the hazards of such chemicals. In addition, cytogenetic studies in the current work revealed the importance of spirulina in ameliorating the genotoxic effects of a mixture of some chemicals used in fracking.
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Abdel-Daim, M.M.; Abuzead, S.M.M.; Halawa, S.M. (2013). Protective role of Spirulina platensis against acute deltamethrin-induced toxicity in rats. PLoS One Sept. 9; 8(9):e72991. doi: https://doi.org/10.1371/journal.pone.0072991
Adel M, Yeganeh S, Dadar M, Sakai M, Dawood MA (2016) Effects of dietary Spirulina platensis on growth performance, humoral and mucosal immune responses and disease resistance in juvenile great sturgeon (Huso Linnaeus, 1754). Fish Shellfish Immunol 56:436–444
Al-Sabti K (1986) Clastogenic effect of five carcinogenic mutagenic chemicals on the cells of the common crab. Comp Biochem Physiol 8:5–9
Au DWT (2004) The application of histo-cytopathological biomarkers in marine pollution monitoring: a review. Mar Pollut Bull 48:817–834
Bamberger M, Oswald RE (2015) Long-term impacts of unconventional drilling operations on human and animal health. J Environ Sci Health A Tox Hazard Subst Environ Eng 50(5):447–459
Bancroft, J.D.; Suyarna, K.; Layton, C. (2012) Bancroft’s theory and practice of histological techniques. 7th ed. E book ISBN: 978-0-7020-5032-9
Belpaeme K, Cooreman K, Kirsch–Volders M (1998) Development and validation of the in vivo alkaline comet assay for detecting genomic damage in marine flatfish. Mutat Res Genet Toxicol 415:167–184
Bills TD, Marking LL, Howe GE (1993) Sensitivity of juvenile striped bass to chemicals used in aquaculture. In: Resour.Publ, vol 192. Fish Wildl. Serv., U.S.D.I., Washington, DC, p 11
Buecker A, Carvalho W, Alves-Gomes JA (2006) Evaluation of mutagenicity and genotoxicity in Eigenmannia virescens (Teleostei, Gymnotiformes) exposed to benzene. Acta Amaz 36:357–364
Buecker A, Carvalho MS, Conceição MB, Alves-Gomes JA (2012) Micronucleus test and comet assay in erythrocytes of the Amazonian electric fish Apteronotus bonapartii exposed to benzene. J Braz Soc Ecotoxicol 7(1):65–73
Chen H, Carter KE (2017) Characterization of the chemicals used in hydraulic fracturing fluids for wells located in the Marcellus Shale Play. J Environ Manag 200:312–324
Chen SS, Sun Y, Tsang DCW, Graham NJD, Ok YS, Feng Y, Li XD (2017) Insights into the subsurface transport of As (V) and Se (VI) in produced water from hydraulic fracturing using soil samples from Qingshankou Formation, Songliao Basin, China. Environ Pollut 223:449–456
Conklin KA (2000) Dietary antioxidants during cancer chemotherapy: impact on chemotherapeutic effectiveness and development of side effects. Nutr Cancer 37(1):1–18
De-Andrade VM, De-Freitas TR, Da Silva J (2004) Comet assay using mullet (Mugil sp.) and sea catfish (Netuma sp.) erythrocytes for the detection of genotoxic pollutants in aquatic environment. Mutat Res 560:57–67
De-Bashan LE, Bashan Y (2010) Immobilized microalgae for removing pollutants: review of practical aspects. Bioresour Technol 101:1611–1627
Duncan PL, Klesius PH (1996) Effects of feeding spirulina on specific and nonspecific immune responses of channel catfish. J Aquat Anim Hlth 8(4):308–313
Egyptian Initiative for Personal Rights (2012) Oil companies in Egypt use controversial technology banned in a number of countries-EIPR warns: gas extraction using hydraulic fracturing threatens Egypt’s water resources. http://eipr.org/en/pressrelease/2012/09/19/1492
Elliott EG, Ettinger AS, Leaderer BP, Bracken M, Deziel NC (2017) A systemic evaluation of chemicals in hydraulic-fracturing fluids and wastewater for reproductive and developmental toxicity. J Expo Sci Environ Epidemiol 27(1):90–99. https://doi.org/10.1038/jes.2015.81
Ezeonyejiaku CD, Obiakor MO, Ezenwelu CO (2011) Toxicity of copper sulphate and behavioral locomotor response of tilapia (Oreochromis niloticus) and catfish (Clarias gariepinus) species. Online J Anim Feed Res 1:130–134
Feldman BF, Zinkl JG, Jain NC (2000) Schalm’s veterinary hematology, 5th edn. Lea and Febiger, Philadelphia, U.S.A., p 1120
Fermanagh Fracking Awareness Network (FFAN) (2012). http://www.frackaware.com/wordpress/wp-content/uploads/2012/08/Fishing-Health-and-What-is-Fracking.pdf
Flores-Lopes F, Thomaz AT (2011) Histopathologic alterations observed in fish gills as a tool in environmental monitoring. Braz J Biol 71(1):179–188
Folkerts EJ, Blewetta TA, He YH, Goss GG (2017) Cardio-respirometry disruption in zebrafish (Danio rerio) embryos exposed to hydraulic fracturing flow back and produced water. Environ Pollut 231(2):1477–1487
Frenzilli G, Lyons BP (2013) The comet assay in marine animals. Methods Mol Biol 1044:363–372
Frenzilli G, Nigro M, Lyons BP (2009) The comet assay for the evaluation of genotoxic impact in aquatic environments. Mutat Res 681:80–92
Gawlik BM, Tavazzi S, Mariani G, Skejo H, Comero S (2017) Analysis of chemical constituents and additives in hydraulic fracturing waters. Joint research Center technical report, Publications Office of the European Union, Luxembourg
Girish KB, Bijoy NS (2014) Copper toxicity: hematological and histopathological changes and prophylactic role of vitamin C in the fish, Anabas testudineus (Bloch, 1792). J Zoo Stud 1(3):4–13
Goss S (2013) Fracking fluids spill caused Kentucky fish kill. http://www.ewg.org/enviroblog/2013/09/fracking-fluids-spill-caused-kentucky-fish-kill-
Greg R, Robert H, Norman J (2004) Unlocking the Monterey Shale potential at Elk Hills: a case study. In SPE international thermal operations and heavy oil symposium and western regional meeting.16-18 March, Bakersfield, California, USA.
Haque SE, Gilani KM (2005) Effect of ambroxol, spirulina and vitamin-E in naphthalyne induced cataract in female rats. Indian J Physiol Pharmacol 49(1):57–64
Harkness JS, Dwyer GS, Warner NR, Parker KM, Mitch WA, Vengosh A (2015) Iodide, bromide, and ammonium in hydraulic fracturing and oil and gas wastewaters: environmental implications. Environ Sci Technol 49(3):1955–1963. https://doi.org/10.1021/es504654n
He Y, Folkerts EJ, Zhang Y, Martin JW, Alessi DS, Goss GG (2017) Effects on biotransformation, oxidative stress, and endocrine disruption in rainbow trout (Oncorhynchus mykiss) exposed to hydraulic fracturing flowback and produced water. Environ Sci Technol 51(2):940–947
He Y, Sun C, Zhang Y, Folkerts EJ, Martin JW, Goss GG (2018) Developmental toxicity of the organic fraction from hydraulic fracturing flowback and produced waters to early life stages of zebrafish (Danio rerio). Environ Sci Technol 52(6):3820–3830
Hirahashi T, Matoto M, Hazeki K, Saeki Y, Ui M, Seya T (2002) Activation of the human innate immune system by spirulina: augmentation of interferon production and NK cytotoxicity by oral administration of hot water extract of Spirulina platensis. Inter Immuno-pharmacol 2:423–434
Hironobu W, Kazuki O, Asmi C, Tassakka T, Masahiro S (2006) Immuno-stimulant effects of dietary Spirulina platensis on carp. Cyprinus carpio Aquac 258:157–163
Kahrilas GA, Blotevogel J, Stewart PS, Thomas-Borch T (2015) Biocides in hydraulic fracturing fluids: a critical review of their usage, mobility, degradation, and toxicity. Environ Sci Technol 49:16–32. https://doi.org/10.1021/es503724k
Kassotis CD, Tillitt DE, Davis JW, Hormann AM, Nagel SC (2014) Estrogen and androgen receptor activities of hydraulic fracturing chemicals, surface and ground water in a drilling-dense region. Endocrinology. 155(3):897–907. https://doi.org/10.1210/en.2013-1697
Kassotis CD, Klemp KC, Vu D, C; Lin C-H, Meng C-X 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. https://doi.org/10.1210/en.2015-1375
Kassotis CD, Nagel SC, Stapleton MH (2018) Unconventional oil and gas chemicals and wastewater-impacted water samples promote adipogenesis via PPARγ-dependent and independent mechanisms in 3T3–L1 cells. Sci Total Environ Nov 01(640-641):1601–1610. https://doi.org/10.1016/j.scitotenv.2018.05.030
Kurashvili M, Varazi T, Khatisashvili G, Gigolashvili G, Adamia G, Pruidze M, Gordeziani M, Chokheli L, Japharashvili S, Khuskivadze N (2018) Blue-green alga spirulina as a tool against water pollution by 1,1′-(2,2,2-trichloroethane-1,1-diyl)bis(4-chlorobenzene) (DDT). Annals Agrarian Sc 16(4):405–409. https://doi.org/10.1016/j.aasci.2018.07.005
Lee RF, Steinert S (2003) Use of the single cell gel electrophoresis/comet assay for detecting DNA damage in aquatic (marine and freshwater) animals. Mutat Res 544:43–64
Leung HW (2001) Ecotoxicology of glutaraldehyde: review of environmental fate and effects studies. Ecotoxicol Environ Saf 49(1):26–39
Lovasoa C (2014) Study of treated and untreated oil based drilling waste using a biomarker approach: gill and liver histopathology in Atlantic salmon (Salmo salar). MSc. Environmental Technology/Offshore Environmental Engineering. In: Faculty of Science and Technology. University of Stavanger, Norway
Luek JL, Gonsior M (2017) A review of organic compounds in hydraulic fracturing fluids and wastewaters. Water Res 123:536–548. https://doi.org/10.1016/j.watres.2017.07.012
Mahmoud MA, Abdelsalam M, Mahdy OA, El Miniawy HMF, Ahmed ZA et al (2016) Infectious bacterial pathogens, parasites and pathological correlations of sewage pollution as an important threat to farmed fishes in Egypt. Environ Pollut 219:939–948
Mall, A. (2014). Halliburton takes 5 days to provide chemical information at Ohio fracking explosion that killed 70,000 fish. NRDC. https://www.nrdc.org/experts/amy-mall/halliburton-takes-5-days-provide-chemical-information-ohio-fracking-explosion.
Martine GR, Loureiro AP, Marques SA, Miyamoto S, Yamaquchi LF (2003) In: Oxidative and alkylating damage in DNA. Mutation Res./Rev. Mutat. Res., 544, (2-3): 115- 127
Mazon AF, Monteiro EAS, Pinheiro GHD, Fernandes MN (2002) Hematological and physiological changes induced by short-term exposure to copper in the freshwater fish. Prochilodusscrofa Braz Biol 62:621–631
McCullough SD, On DM, Bowers EC (2017) Using chromatin immunoprecipitation in toxicology: a step-by-step guide to increasing efficiency, reducing variability, and expanding applications. Curr Protoc Toxicol 2; 72:3.14.1-3.14.28. https://doi.org/10.1002/cptx.22
McKenzie LM, Witter RZ, Newman LS, Adgate JL (2012) Human health risk assessment of air emissions from development of unconventional natural gas resources. Sci Total Environ 424:79–87
Morgan RD (2012) What the frack? An empirical analysis of the effect of regulation on hydraulic fracturing. Quinnipiac Hlth Law J 16(1):77–114
Nascimento AA, Arau’jo FG, Gomes ID, Mendes RMM, Sales A (2012) Fish gills alterations as potential biomarkers of environmental quality in a eutrophized tropical river in South-Eastern Brazil. Anat Histol Embryol 41:209–216
National Institute of health (NIH) (2016) https://pubchem.ncbi.nlm.nih.gov/compound/Ammonium_persulfate#section=Non-Human-Toxicity-Values
Papoulias DM, Velasco A (2013) Histopathological analysis of fish from Acorn Fork Creek, Kentucky, exposed to hydraulic fracturing fluid releases. Southeast Nat (12):92–111
Prahalathan C, Selvakumar E, Varalakshmi P (2006) Lipoic acid modulates Adriamycin induced testicular toxicity. Reprod Toxicol 21:54–59
Praveen N, Shadab GA (2012) Cytogenetic evaluation of cadmium chloride on Channa punctatus. J Environ Biol 33:663–666
Premkumar K, Pachiappan A, Abraham SK, Santhiya ST, Gopinata PM, Ramesh A (2001) Effect of Spirulina fusiformis on cyclophosphamide and mitomycin-C induced genotoxicity and oxidative stress in mice. Fitoterapia 72:906–911
Rahman K (2007) Studies on free radicals, antioxidants, and co-factors. Clinic Inter Aging 2(2):219–236
Ray J, Peterson DA, Schinstine M, Gage FH (1993) Proliferation, differentiation, and long-term culture of primary hippocampal neurons. Proc Natl Acad Sci 90:3602–3606
Ray S, Roy K, Sengupta C (2007) Evaluation of protective effects of water extract of spirulina platensis (blue green algae) on cisplatin-induced lipid peroxidation. Indian J Pharm Sci 69:378–383
Roja SJ, Abbas B, Maryam G, Seyed MV, Maryam T (2013) Impact of copper sulphate on hematological and some biochemical parameters of common Carp (Cyprinus carpio L., 1758) in different pH. World J. Fish & Marine Sc 5(5):486–491
Shelke AD, Wani GP (2015) Protective effect of dietary supplementation of Spirulina platensis on improvement of growth parameters in mercuric chloride exposed fish. Int J of Life Science (A3):38–41
Singh D, Nath K, Trivedi SP, Sharma YK (2008) Impact of copper on hematological profile of freshwater fish, Channa punctatus. J Environ Biol 29:253–257
Srivastava S, Gupta A, Chaturvedi S, Abhinav A, Singh R (2009) Effects of short-term therapeutic bath of malachite green and formalin on certain hematological parameters of a freshwater catfish, (Heteropneustes fossilis) (Bloch). J Exp Zool 12(1):79–83
Tao XY, Yu SY, Kang L, Huang HX, Wei AY (2004) Study on the genetic damage in mice induced by the volatile organic compounds of decoration materials. Zhonghua Lao Dong Wei Sheng Zhi Ye Bing ZaZhi, 22: 194-196
Tavares-Dias M, Martins ML, Schalch SH, Onaka CIF, Quintana JRE et al (2002) Hematologic and histopathologic changes in pacu (Piaractusmes opotamicus) Holmberg, 1887 (Osteichthyes, Characidae) treated with copper sulfate (CuSO4). Acta Scientiarum Maringá 24(2):547–554
United States House of Representatives. “US House of Representative” (2011). Chemicals used in hydraulic fracturing. Washington, DC: Committee on Energy and Commerce APRIL 2011
Višnjić-Jeftić Z, Jarić I, Jovanovic L et al (2010) Heavy metal and trace element accumulation in muscle, liver and gills of the Pontic shad (Alosa immaculata Bennet 1835) from the Danube River (Serbia). Microchem J 95(2):341–344
Vutukuru S, Suma C, Madhavi K, Juveria S, Pauleena J, Raoand J, Anjaneyulu Y (2005) Studies on the development of potential biomarkers for rapid assessment of copper toxicity to freshwater fish using Esomusdanricus as model. Int J Environ Res Public Health 2(1):63–73
Wannee JK, Somphong S (2007) Efficacy of ascorbic acid reducing water bone copper toxicity in butterfish (Poronotus triacanthus). J Biol Sci 7:620–625
Wattenberg EV, Bielicki JM, Suchomel AE, Sweet JT, Vold EM, Ramachandran G (2015) Assessment of the acute and chronic health hazards of hydraulic fracturing fluids. J Occup Environ Hyg 12(9):611–624. https://doi.org/10.1080/15459624.2015.1029612
Whysner J, Reddy MV, Ross PM, Mohan M, Lax EA (2004) Genotoxicity of benzene and its metabolites. Mutat Res 566:99–130
World Health Organization (2016) http://monographs.iarc.fr/ENG/Classification/index.php
Xu J, Lian LJ, Wu C, Wang XF, Fu WY, Xu LH (2008) Lead induces oxidative stress, DNA damage and alteration of p53, Bax and Bcl-2 expressions in mice. Food Chem Toxicol 46(5):1488–1494
Yadav KK, Trivedi SP (2009) Chromosomal aberrations in a fish Channa punctatus after in vivo exposure to three heavy metals. Mutation Res Gen Toxicol Environ Mut 1:7–12
Yesudass T, Sekar J, Muthusamy P (2014) Effect of copper toxicity on hematological parameters to fresh water fish Cyprinus Carpio (Common Carp). J Environ Sci Toxicolo Food Technology 8:50–60
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The authors would like to express their gratitude to Prof. R. Tolba, director of the Department for Laboratory Animal Science, and Dr. J. Steitz and Dr. P. K. Srinivasan at the Department for Laboratory Animal Science, University Hospital, RWTH Aachen, Germany, for their continuous encouragement, valuable advice, and help in the production of this article.
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Mahmoud, M.A., Abd El-Rahim, A.H., Mahrous, K.F. et al. The impact of several hydraulic fracking chemicals on Nile tilapia and evaluation of the protective effects of Spirulina platensis. Environ Sci Pollut Res 26, 19453–19467 (2019). https://doi.org/10.1007/s11356-019-05246-3
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DOI: https://doi.org/10.1007/s11356-019-05246-3