Abstract
Polycyclic aromatic hydrocarbons (PAHs) are a family of contaminants that consist of two or more aromatic rings fused together. Soils contaminated with PAHs pose significant risk to human and ecological health. Over the last 50 years, significant research has been directed towards the cleanup of PAH-contaminated soils to background level. However, this achieved only limited success especially with high molecular weight compounds. Notably, during the last 5–10 years, the approach to remediate PAH-contaminated soils has changed considerably. A risk-based prioritization of remediation interventions has become a valuable step in the management of contaminated sites. The hydrophobicity of PAHs underlines that their phase distribution in soil is strongly influenced by factors such as soil properties and ageing of PAHs within the soil. A risk-based approach recognizes that exposure and environmental effects of PAHs are not directly related to the commonly measured total chemical concentration. Thus, a bioavailability-based assessment using a combination of chemical analysis with toxicological assays and nonexhaustive extraction technique would serve as a valuable tool in risk-based approach for remediation of PAH-contaminated soils. In this paper, the fate and availability of PAHs in contaminated soils and their relevance to risk-based management of long-term contaminated soils are reviewed. This review may serve as guidance for the use of site-specific risk-based management methods.
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References
Alexander M (1991) Research needs in bioremediation. Environ Sci Technol 25:1972–1973
Alexander M (2000) Aging, bioavailability, and overestimation of risk from environmental pollutants. Environ Sci Technol 34:4259–4265
Atagana HI (2004) Bioremediation of creosote-contaminated soil in South Africa by landfarming. J Appl Microbiol 96:510–520
ATSDR (Agency for Toxic Substances and Disease Registry) (1995) Toxicological profile for polycyclic aromatic hydrocarbons. US Department of Health and Human Service, ATSDR, Atlanta
Baldi F, Leonardi V, D’Annibale A, Piccolo A, Zecchini F, Petruccioli M (2007) Integrated approach of metal removal and bioprecipitation followed by fungal degradation of organic pollutants from contaminated soils. Eur J Soil Biol 43:380–387
Bamforth SM, Singleton I (2005) Bioremediation of polycyclic aromatic hydrocarbons: current knowledge and future directions. J Chem Technol Biotech 80:723–736
Beck AJ, Wilson SC, Alcock RE, Jones KC (1995) Kinetic constraints on the loss of organic chemicals from contaminated soils: implications for soil-quality limits. Crit Rev Environ Sci Technol 25:1–43
Bosma TNP, Middeldorp PJM, Schraa G, Zehnder AJB (1996) Mass transfer limitation of biotransformation: quantifying bioavailability. Environ Sci Technol 31:248–252
Catney P, Henneberry J, Meadowcroft J, Eiser JR (2006) Dealing with contaminated land in the UK through ‘Developmental Managerialism’. J Environ Policy Plan 8:331–356
Cerniglia CE (1992) Biodegradation of polycyclic aromatic hydrocarbons. Biodegradation 3:351–368
Chiou CT, MCGroddy SE, Kile DE (1998) Partition characteristics of polycyclic aromatic hydrocarbons on soils and sediments. Environ Sci Technol 32:264–269
Cho Y-M, Ghosh U, Kennedy AJ, Grossman A, Ray G, Tomaszewski JE, Smithenry DW, Bridges TS, Luthy RG (2009) Field application of activated carbon amendment for in situ stabilisation of polychlorinated biphenyls in marine sediment. Environ Sci Technol 43:3815–3823
Christman RF, Pfaender FK (2006) Molecular implications of hydrophobic organic partitioning theory. Acta Hydrochim Hydrobiol 34:367–374
Chung NH, Alexander M (1998) Differences in sequestration and bioavailability of organic compounds aged in dissimilar soils. Environ Sci Technol 32:855–860
Chung NH, Alexander M (2002) Effect of soil properties on bioavailability and extractability of phenanthrene and atrazine sequestered in soil. Chemosphere 48:109–115
Coover MP, Sims RC (1987) The effect of temperature on polycyclic aromatic hydrocarbon persistence in an unacclimated agricultural soil. Hazard Waste Hazard Mater 4:69–82
Cornelissen G, Rigterink H, Ferdinandy MMA, van Noort PCM (1998) Rapidly desorbing fractions of PAHs in contaminated sediments as a predictor of the extent of bioremediation. Environ Sci Technol 32:966–970
Cornelissen G, Gustafsson O, Bucheli TD, Jonker MTO, Koelmans AA, Van Noort PCM (2005) Extensive sorption of organic compounds to black carbon, coal, and kerogen in sediments and soils: mechanisms and consequences for distribution, bioaccumulation, and biodegradation. Environ Sci Technol 39:6881–6895
Cui X, Mayer P, Gan J (2013) Methods to assess bioavailability of hydrophobic organic contaminants: principles, operation and limitations. Environ Pollut 172:223–234
Cuypers C, Grotenhuis T, Joziasse J, Rulkens W (2000) Rapid persulfate oxidation predicts PAH bioavailability in soils and sediments. Environ Sci Technol 34:2057–2063
Cuypers C, Pancras T, Grotenhuis T, Rulkens W (2002) The estimation of PAH bioavailability in contaminated sediments using hydroxypropyl-[beta]-cyclodextrin and Triton X-100 extraction techniques. Chemosphere 46:1235–1245
Cvancarova M, Kresinova Z, Cajthaml T (2013) Influence of the bioaccessible fraction of polycyclic aromatic hydrocarbons on the ecotoxicity of historically contaminated soils. J Hazard Mater 254–255:116–124
Das K, Mukherjee AK (2007) Differential utilization of pyrene as the sole source of carbon by Bacillus subtilis and Pseudomonas aeruginosa strains; role of biosurfactants in enhancing bioavailability. J Appl Microbiol 102:195–203
EEA (2007) Europe’s environment—the fourth assessment. State of the environment report 2007, European Environment Agency
Ehrlich GG, Goerlitz DF, Godsy EM, Hult MF (1982) Degradation of phenolic contaminants in ground water by anaerobic bacteria: St. Louis Park, Minnesota. Groundw 20:703–710
Erickson DC, Loehr RC, Neuhauser EF (1993) PAH loss during bioremediation of manufactured gas plant site soils. Water Res 27:911–919
Gardner WS, Lee RF, Tenore KR, Smith LW (1979) Degradation of selected polycyclic aromatic hydrocarbons in coastal sediments: importance of microbes and polychaete worms. Water Air Soil Pollut 11:339–347
Gauthier TD, Siitz WR, Grant CL (1987) Effects of structural and compositional variations of dissolved humic materials on pyrene K oc values. Environ Sci Technol 21:243–248
Ghosh U, Zimmerman JR, Luthy RG (2003) PCB and PAH speciation among particle types in contaminated harbor sediments and effects on PAH bioavailability. Environ Sci Technol 37:2209–2217
Ginn JS, Doucette WJ, Sims RC (1994) Chemical mass-balance approach for estimating fate and transport of polycyclic aromatic metabolites in the subsurface environment. Polycycl Aromat Compd 5:225–234
Guerin WF, Boyd SA (1997) Bioavailability of naphthalene associated with natural and synthetic sorbents. Water Res 31:1504–1512
Haeseler F, Blanchet D, Druelle V, Werner P, Vandecasteele J-P (1999) Ecotoxicological assessment of soils of former manufactured gas plant sites: bioremediation potential and pollutant mobility. Environ Sci Technol 33:4379–4384
Haritash AK, Kaushik CP (2009) Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): a review. J Hazard Mater 169:1–15
Harmsen J (2007) Measuring bioavailability: from a scientific approach to standard methods. J Environ Qual 36:1420–1428
Hawthorne SB, Grabanski CB (2000) Correlating selective supercritical fluid extraction with bioremediation behavior of PAHs in a field treatment plot. Environ Sci Technol 34:4103–4110
Hu J, Nakamura J, Richardson SD, Aitken MD (2012) Evaluating the effects of bioremediation on genotoxicity of polycyclic aromatic hydrocarbon-contaminated soil using genetically engineered, higher eukaryotic cell lines. Environ Sci Technol 46:4607–4613
Hubalek T, Vosahlova S, Mateju V, Kovacova N, Novotny C (2007) Ecotoxicity monitoring of hydrocarbon-contaminated soil during bioremediation: a case study. Arch Environ Contam Toxicol 52:1–7
Huckins JN, Tubergen MW, Manuweera GK (1990) Semipermeable membrane devices containing model lipid: a new approach to monitoring bioavailability of lipophilic contaminants and estimating their bioconcentration potential. Chemosphere 20:533–552
Huesemann MH, Hausmann TS, Fortman TJ (2004) Does bioavailability limit biodegradation? A comparison of hydrocarbon biodegradation and desorption rates in aged soils. Biodegradation 15:261–274
Huesmann MH, Rhodes IA, Rice-Jackson LM, Sterna LL, Moore KO (1995) Changes in hydrocarbon composition during slurry bioremediation of diesel-based drill cuttings. In: Proceedings of IGTs 6th International Symposium on Gas, Oil and Environmental Biotechnology, Colorado Springs, CO, pp 97–118
Johnsen AR, de Lipathay JR, Sorensen SJ, Ekelund F, Christensen P, Andersen O, Karlson U, Jacobsen CS (2006) Microbial degradation of street dust polycyclic aromatic hydrocarbons in microcosms simulating diffuse pollution of urban soil. Environ Microbiol 8:535–545
Johnson MD, Weber WJ (2001) Rapid prediction of long-term rates of contaminant desorption from soils and sediments. Environ Sci Technol 35:427–433
Jones KC, Stratford JA, Tidridge P, Waterhouse KS (1989) Polynuclear aromatic hydrocarbons in an agricultural soil: long-term changes in profile distribution. Environ Pollut 56:337–351
Juhasz AL, Naidu R (2000) Bioremediation of high molecular weight polycyclic aromatic hydrocarbons: a review of the microbial degradation of benzo[a]pyrene. Int Biodeterior Biodegrad 45:57–88
Karickhoff SW, Brown DS, Scott TA (1979) Sorption of hydrophobic pollutants on natural sediments. Water Res 13:241–248
Lee SJ, Pardue JH, Moe WM, Kim DJ (2009) Effect of sorption and desorption-resistance on biodegradation of chlorobenzene in two wet land soils. J Hazard Mat 161:492–498
Loehr RC (1996) The environmental impact of soil contamination: bioavailability, risk assessment, and policy implications. Policy Study 211. Reason Foundation, Los Angeles
Luo L, Lin S, Huang H, Zhang S (2012) Relationships between aging of PAHs and soil properties. Environ Pollut 170:177–182
Mackay D, Callcott D (1998) Partitioning and physical chemical properties of PAHs. In: Neilson AH (ed) The handbook of environmental chemistry: PAHs and related compounds. Springer, New York, pp 325–346
Maxin CR, Kogel-Knabner I (1995) Partitioning of polycyclic aromatic hydrocarbons (PAH) in water soluble soil organic matter. Eur J Soil Sci 46:193–204
Megharaj M, Singleton I, McClure NC, Naidu R (2000) Influence of petroleum hydrocarbon contamination on microalgae and microbial activities in a long-term contaminated soil. Arch Environ Contam Toxicol 38:439–445
Megharaj M, Ramakrishnan B, Venkateswarlu K, Sethunathan N, Naidu R (2011) Bioremediation approaches for organic pollutants: a critical perspective. Environ Int 37:1362–1375
Mumtaz M, George J (1995) Toxicological profile for polycyclic aromatic hydrocarbons. US Dept of Health and Human Services, Agency for Toxic Substances and Disease Registry, Atlanta
Naidu R, Bolan NS (2008) Contaminant chemistry in soils: key concepts and bioavailability. In: Naidu R et al. (ed) Developments in soil science, vol 32. Elsevier BV, Amsterdam, pp. 9–37
Naidu R, Kookana RS, Sumner ME, Harter RD, Tiller KG (1997) Cadmium sorption and transport in variable charge soil: a review. J Environ Qual 26:602–617
Naidu R, Pollard SJT, Bolan NS, Owens G, Pruszinski AW (2008) Bioavailability: the underlying basis for risk based land management. In: Naidu et al (eds) Chemical bioavailability in terrestrial environment. Elsevier, Amsterdam, pp 53–72
Nam K, Alexander M (1998) Role of nanoporosity and hydrophobicity in sequestration and bioavailability: tests with model solids. Environ Sci Technol 32:71–74
Nathanail CP, Earl N (2001) Human health risk assessment: guideline values and magic numbers. Issues Environ Sci Technol 16:85–102
NEPM-ASC (1999) National environmental protection measure for assessment of site contamination. National Environmental Protection Council, Commonwealth of Australia, Canberra
Nopcharoenkul W, Pinphanichakarn P, Pinyakong O (2011) The development of a liquid formulation of Pseudoxanthomonas sp. RN402 and its application in the treatment of pyrene-contaminated soil. J Appl Microbiol 111:36–47
NRC (2003) Bioavailability of contaminants in soils and sediments: processes, tools and applications. The National Academic Press, Washington, DC
O’Berg T, Bergback B (2005) A review of probabilistic risk assessment of contaminated land. J Soils Sediments 5:213–224
Park KS, Sims RC, Dupont RR, Doucette WJ, Matthews JE (1990) Fate of PAH compounds in two soil types: Influence of volatilization, abiotic loss and biological activity. Environ Toxicol Chem 9:187–195
Park JH, Feng Y, Cho SY, Voice TC, Boyd SA (2004) Sorbed atrazine shifts into non-desorbable sites of soil organic matter during aging. Water Res 38:3881–3892
Pignatello JJ, Xing BS (1996) Mechanisms of slow sorption of organic chemicals to natural particles. Environ Sci Technol 30:1–11
Potin O, Veignie E, Rafin C (2004) Biodegradation of polycyclic aromatic hydrocarbons (PAHs) by Cladosporium sphaerospermum isolated from an aged PAH contaminated soil. FEMS Microbiol Ecol 51:71–78
Reid BJ, Stokes JD, Jones KC, Semple KT (2000a) Nonexhaustive cyclodextrin-based extraction technique for the evaluation of PAH bioavailability. Environ Sci Technol 34:3174–3179
Reid BJ, Jones KC, Semple KT (2000b) Bioavailability of persistent organic pollutants in soils and sediments—a perspective on mechanisms, consequences and assessment. Environ Pollut 108:103–112
Rhodes AH, Carlin A, Semple KT (2008) Impact of black carbon in the extraction and mineralisation of phenanthrene in soil. Environ Sci Technol 42:740–745
Rila J-P, Eisentraeger A (2003) Application of bioassays for risk characterisation and remediation control of soils polluted with nitroaromatics and PAHs. Wat Air Soil Pollut 148:223–242
Rothstein H, Irving P, Walden T, Yearsley R (2006) The risks of risk-based regulation: insights from the Environmental Policy Domain. Environ Int 32:1056–1065
Rulkens WH, Grotenhuis JTC, Harmsen J, Sims RC (2004) Physical/chemical measurements of bioavailability: function in the selection of soil remediation strategies. In: Proceedings of the seventh international in situ and on site bioremediation symposium (Orlando, Fl. June 2000). Columbus OH, Battelle Press, USA
Saison C, Perrin-Ganier C, Schiavon M, Morel J (2004) Effect of cropping and tillage on the dissipation of PAH contamination in soil. Environ Pollut 130:275–285
Semple KT, Doick KJ, Jones KC, Burauel P, Craven A, Harms H (2004) Defining bioavailability and bioaccessibility of contaminated soil and sediment is complicated. Environ Sci Technol 38:228A–231A
Sims RC, Overcash M (1983) Fate of polynuclear aromatic-compounds (PAHs) in soil–plant systems. Residue Rev 88:1–68
Sims RC, Doucette WJ, McLean JE, Grenney WJ, Dupont RR (1988) Treatment potential for 56 EPA listed hazardous chemicals in soil. Robert Kerr Environmental Research Laboratory, Ada
Singh N, Megharaj M, Gates WP, Churchman GJ, Anderson JA, Kookana RS, Naidu R, Chen Z, Slade PG, Sethunathan N (2003) Bioavailability of an organophosphorus pesticide, fenamiphos, sorbed on an organo-clay. J Agric Food Chem 51:2653–2658
Singh N, Sethunathan N, Megharaj M, Naidu R. (2008) Bioavailability of sorbed pesticides to bacteria: an overview. In: Naidu R et al. (ed) Developments in soil science, vol 32. Elsevier BV, Amsterdam, pp. 71–80
Sofuoglu A, Odabasi M, Tasdemir Y, Khalili NR, Holsen TM (2001) Temperature dependence of gas-phase polycyclic aromatic hydrocarbon and organochlorine pesticide concentrations in Chicago air. Atmos Environ 35:6503–6510
Southworth GR (1979) The role of volatilization in removing polycyclic aromatic hydrocarbons from aquatic environments. Bull Environ Contam Toxicol 21:507–514
Stroo HF, Jensen R, Loehr RC, Nackles DV, Fairbrother A, Liban CB (2000) Environmentally acceptable endpoints for PAHs at a manufactured gas plant site. Environ Sci Technol 34:3831–3836
Stroud JL, Paton GI, Semple KT (2007) Microbe-aliphatic hydrocarbon interactions in soil: implications for biodegradation and bioremediation. J Appl Microbiol 102:1239–1253
Tang WC, White JC, Alexander M (1998) Utilisation of sorbed compounds by microorganisms specially isolated for that purpose. Appl Microbiol Biotechnol 49:117–121
Thavamani P, Megharaj M, McFarland R, Naidu R (2011) Finger printing of mixed contaminants from former manufactured gas plant (MGP) site soils: implications to bioremediation. Environ Int 37:184–189
Thavamani P, Megharaj M, Naidu R (2012) Bioremediation of high molecular weight polyaromatic hydrocarbons co-contaminated with metals in liquid and soil slurries by metal tolerant PAHs degrading bacterial consortium. Biodegradation 23:823–835
Thavamani P, Megharaj M, Venkateswarlu K, Naidu R (2013) Mixed contamination of polyaromatic hydrocarbons and metals at manufactured gas plant sites: toxicity and implications to bioremediation. In: Wong MH (ed) Environmental contamination—health risks, bioavailability and bioremediation. Taylor and Francis, New York, pp. 347–368
Tucker B, McLean JE, Brar JS, Anderson AJ (1995) Soil composition and suppression of pyrene mineralisation by Phanerochate chrysosporium. In: Erickson LE, Tillison DE, Grant SC, McDonald JP (eds) Proceedings of 10th annual conference on hazardous waste research, Kansas State University, Manhatton, Kansas, USA, pp 325–332
Venkata Mohan S, Kisa T, Ohkuma T, Kanaly RA, Shimizu Y (2006) Bioremediation technologies for treatment of PAH-contaminated soil and strategies to enhance process efficiency. Rev Environ Sci Biotechnol 5:347–374
Weissenfels WD, Klewer H-J, Langhoff J (1992) Adsorption of polycyclic aromatic hydrocarbons (PAHs) by soil particles: influence on biodegradability and biotoxicity. Appl Microbiol Biotechnol 36:689–696
Wild S, Jones K (1993) Biological and abiotic losses of polynuclear aromatic hydrocarbons (PAHs) from soils freshly amended with sewage sludge. Environ Toxicol Chem 12:5–12
Wilson SC, Jones KC (1993) Bioremediation of soil contaminated with polynuclear aromatic-hydrocarbons (PAHs)—a review. Environ Pollut 81:229–249
Wilson JT, McNabb JF, Cochran JW, Wang TH, Tomson MB, Bedient PB (1985) Influence of microbial adaptation on the fate of organic pollutants in ground water. Environ Toxicol Chem 4:721–726
Wu SC, Gschwend PM (1986) Sorption kinetics of hydrophobic organic-compounds compounds to natural sediments and soil. Environ Sci Technol 20:717–725
Yang Y, Hunter W, Tao S (2009) Microbial availability of different forms of phenanthrene in soils. Environ Sci Technol 43:1852–1857
Yang Y, Zhang N, Xue M, Lu ST, Tao S (2011) Effects of soil organic matter on the development of the microbial polycyclic aromatic hydrocarbons (PAHs) degradation potentials. Environ Pollut 159:591–595
Zhang Y, Wang F, Bian Y, Kengara FO, Gu C, Zhao Q, Jiang X (2012) Enhanced desorption of humin-bound phenanthrene by attached phenanthrene-degrading bacteria. Bioresour Technol 123:92–97
Zimmerman AR, Chorover J, Goyne KW, Brantley SL (2004) Protection of mesopore-adsorbed organic matter from enzymatic degradation. Environ Sci Technol 38:4542–4548
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Duan, L., Naidu, R., Thavamani, P. et al. Managing long-term polycyclic aromatic hydrocarbon contaminated soils: a risk-based approach. Environ Sci Pollut Res 22, 8927–8941 (2015). https://doi.org/10.1007/s11356-013-2270-0
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DOI: https://doi.org/10.1007/s11356-013-2270-0