Skip to main content

Advertisement

Log in

Polycyclic Aromatic Hydrocarbons: A Critical Review of Environmental Occurrence and Bioremediation

  • Published:
Environmental Management Aims and scope Submit manuscript

Abstract

The degree of polycyclic aromatic hydrocarbon contamination of environmental matrices has increased over the last several years due to increase in industrial activities. Interest has surrounded the occurrence and distribution of polycyclic aromatic hydrocarbons for many decades because they pose a serious threat to the health of humans and ecosystems. The importance of the need for sustainable abatement strategies to alleviate contamination therefore cannot be overemphasised, as daily human activities continue to create pollution from polycyclic aromatic hydrocarbons and impact the natural environment. Globally, attempts have been made to design treatment schemes for the remediation and restoration of contaminated sites. Several techniques and technologies have been proposed and tested over time, the majority of which have significant limitations. This has necessitated research into environmentally friendly and cost-effective clean-up techniques. Bioremediation is an appealing option that has been extensively researched and adopted as it has been proven to be relatively cost-effective, environmentally friendly and is publicly accepted. In this review, the physicochemical properties of some priority polycyclic aromatic hydrocarbons, as well as the pathways and mechanisms through which they enter the soil, river systems, drinking water, groundwater and food are succinctly examined. Their effects on human health, other living organisms, the aquatic ecosystem, as well as soil microbiota are also elucidated. The persistence and bioavailability of polycyclic aromatic hydrocarbons are discussed as well, as they are important factors that influence the rate, efficiency and overall success of remediation. Bioremediation (aerobic and anaerobic), use of biosurfactants and bioreactors, as well as the roles of biofilms in the biological treatment of polycyclic aromatic hydrocarbons are also explored.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Agency for Toxic Substances and Disease Registry (ATSDR) (1995) Toxic Substances Portal-Polycyclic Aromatic Hydrocarbons (PAHs) Public Health Statement for Polycyclic Aromatic Hydrocarbons (PAHs). www.atsdr.cdc.gov/phs/phs.asp?id=120&tid=25

  • Agency for Toxic Substances and Disease Registry (ATSDR). (2011). Toxic Substances-Polycyclic Aromatic Hydrocarbons (PAHs).”ATSDR home web http://www.atsdr.cdc.gov/substances/toxsubstance.asp?toxid=25. Accessed 6 Oct 2014

  • Al-Daher R, Al-Awadhi N, El-Nawawy A (1998) Bioremediation of damaged desert environment using the windrow soil pile system in Kuwait. Environ Int 24:175–180

    Article  CAS  Google Scholar 

  • Alexander M (1999) Biodegradation and bioremediation. Gulf Professional Publishing. 2nd Edition. CA, USA. ISBN: 9780120498611, p 141–176

  • Anastasi A, Tigini V, Varese GC (2013) The bioremediation potential of different ecophysiological groups of fungi. In: Goltapeh EM, Danesh YR, Varma A (eds) Fungi as bioremediators. Springer, Berlin, p 29–49

    Chapter  Google Scholar 

  • Anderson RT, Lovley DR (1997) Ecology and biogeochemistry of in situ groundwater remediation. Adv Microbial Ecol 15:289–350

    CAS  Google Scholar 

  • Annweiler E, Richnow HH, Antranikian G, Hebenbrock S, Garms C, Franke S, Francke W, Michaelis W (2000) Naphthalene degradation and incorporation of naphthalene-derived carbon into biomass by the thermophilic Bacillus thermoleovorans. Appl Environ Microbiol 66:518–523

    Article  CAS  Google Scholar 

  • Arun K, Ashok M, Rajesh S (2010) Crude oil PAH constitution, degradation pathway and associated bioremediation microflora: an overview. Int J Environ Sci 1(7):11–22

    Google Scholar 

  • Arey J, Atkinson R (2003) Photochemical reactions of PAHs in the atmosphere. In: Douben PET (ed) PAHs: an ecotoxicological perspective. Wiley: West Sussex, UK, p 47–63

  • Atanu KJ, Mahalakshmi DK, Sridhari G (2011) Integrated application of bioprocess engineering and biotechniques for quality & bulk drug manufacturing. J Bioequiv Availab 11:3–11

    Google Scholar 

  • Atlas RM, Bartha R (1987) Microbial ecology: fundamentals and applications, 2nd edn. Benjamin/Cummings Publ.Co. Inc, Menlo park, CA, p 412–416

    Google Scholar 

  • Baek SO, Field RA, Goldstone ME, Kirk PW, Lester JN, Perry R (1991) A review of atmospheric polycyclic aromatic hydrocarbons: sources, fate and behavior. Water Air Soil Pollut 60:79–300

    Article  Google Scholar 

  • Baird SJ, Bailey EA, Vorhees DJ (2007) Evaluating human risk from exposure to alkylated PAHs in an aquatic system. Hum Ecol Risk Asses 13(2):322–338

    Article  CAS  Google Scholar 

  • Bamforth SM, Singleton I (2005) Bioremediation of polycyclic aromatic hydrocarbons: current knowledge and future directions. J Chem Technol Biotechnol 80:723–736

    Article  CAS  Google Scholar 

  • Bandowe BAM, Meusel H, Huang RJ, Ho K, Cao J, Hoffmann T, Wilcke W (2014) PM 2.5-bound oxygenated PAHs, nitro-PAHs and parent-PAHs from the atmosphere of a Chinese megacity: seasonal variation, sources and cancer risk assessment. Sci Total Environment 473:77–87

    Article  CAS  Google Scholar 

  • Bakermans C, Hohnstock-Ashe AM, Padmanabhan S, Padmanabhan P, Madsen EL (2002) Geochemical and physiological evidence for mixed aerobic and anaerobic field biodegradation of coal tar waste by subsurface microbial communities. Microb Ecol 44:107–117

    Article  CAS  Google Scholar 

  • Baran S, Bielinska JE, Oleszcuzuka P (2004) Enzymatic activity in an airfield soil polluted with polycyclic aromatic hydrocarbons. Geoderma 118:221–232

    Article  CAS  Google Scholar 

  • Barron MG, Carls MG, Short JW, Rice SD (2003) Photoenhanced toxicity of aqueous phase and chemically dispersed, weathered Alaska North Slope crude oil to Pacific herring eggs and larvae. Environ Toxicol Chem 22:650–660

    Article  CAS  Google Scholar 

  • Barret M, Carrère H, Delgadillo L, Patureau D (2010) PAH fate during the anaerobic digestion of contaminated sludge: Do bioavailability and/or co-metabolism limit their biodegradation? Water Res 44(13):3797–3806

    Article  CAS  Google Scholar 

  • Baumard P, Budzinski H, Garrigues P (1998a) Polycyclic aromatic hydrocarbons in sediments and mussels of the western Mediterranean Sea. Environ Toxicol Chem 17(5):765–776

    Article  CAS  Google Scholar 

  • Baumard P, Budzinski H, Garrigues P, Sorbe JC, Burgeot T, Bellocq J (1998b) Concentrations of PAHs (polycyclic aromatic hydrocarbons) in various marine organisms in relation to those in sediments and to trophic level. Mar Poll Bull 36(12):951–960

    Article  CAS  Google Scholar 

  • Baumard P, Budzinski H, Garrigues P, Dizer H, Hansen PD (1999) Polycyclic aromatic hydrocarbons in recent sediments and mussels (Mytilus edulis) from the Western Baltic Sea: occurrence, bioavailability and seasonal variations. Mar Environ Res 47(1):17–47

    Article  CAS  Google Scholar 

  • Bayoumi RA (2009) Bacterial bioremediation of polycyclic aromatic hydrocarbons in heavy oil contaminated soil. J Appl Sci Res 5(2):197–211

    Google Scholar 

  • Beasley G, Kneale P (2002) Reviewing the impact of metals and PAHs on macro-invertebrates in urban watercourses. Prog Phys Geogr 26(2):236–270

    Article  Google Scholar 

  • Beazley M, Martinez R, Rajan S, Powell J, Piceno Y, Tom L, Anderson G, Hazen T, Nostrand J, Zhou J, Mortazavi B, Sobecky P (2012) Microbial community analysis of a coastal salt marsh affected by the Deepwater horizon oil spill. PloS ONE 7(7):e41305. doi:10.1371/journal.pone.0041305

    Article  CAS  Google Scholar 

  • Benedek T, Vajna B, Tancsics A, Mariaaligeti K, Lanyi S, Mathe I (2013) Remarkable impact of PAHs and TPHs on the richness and diversity of bacterial species in surface soils exposed to long term hydrocarbon pollution. World J Microbiol Biotechnol 29(11):1989–2002

    Article  CAS  Google Scholar 

  • Beyer J, Sandvik M, Hylland K, Fjeld E, Egaas E, Aas E, Skare JU, Goksøyr A (1996) Contaminant accumulation and biomarker responses in flounder (Platichthys flesus L) and Atlantic cod (Gadus morhua L) exposed by caging to polluted sediments in Sørfjorden, Norway. Aquat Toxicol 36(1–2):75–98

    Article  CAS  Google Scholar 

  • Bhattacharya S, Angayarkanni J, Das A, Palaniswamy M (2012) Mycoremediation of benzo(a)pyrene by Pleurotus ostreatus isolated from Wayanad district in Kerala, India. IOSR J Pharm Biol Sci 2(2):84–93

    CAS  Google Scholar 

  • Bhatnagar S, Kumari R (2013) Bioremediation: A sustainable tool for environmental management; a review. Annu Rev Res Bio 3(4):974–993

    CAS  Google Scholar 

  • Boonchan S, Britz ML, Stanley GA (2000) Degradation and mineralization of High-Molecular-Weight polycyclic aromatic hydrocarbons by defined fungal-bacterial cocultures. Appl Environ Microbiol 66(3):1007–1019

    Article  CAS  Google Scholar 

  • Bosma TNP, Middeldorp PJM, Schraa G, Zehnder AJB (1997) Mass transfer limitation of biotransformation: quantifying bioavailability. Environ Sci Technol 31(1):248–252

    Article  CAS  Google Scholar 

  • Borde X, Guieysse B, Delgado O, Munnoz R, Hatti-Kaul R, Nugier-Chauvin C, Patin H, Mattiasson B (2003) Synergistic relationships in algal–bacterial microcosms for the treatment of aromatic pollutants. Bioresour Technol 86:293–300

    Article  Google Scholar 

  • Brinkworth LC, Hodson PV, Tabash S, Lee P (2003) CYP1A induction and blue sac disease in early developmental stages of rainbow trout (Oncorhynchus mykiss) exposed toretene. J Toxicol Environ Health 66A:627–646

    Article  Google Scholar 

  • Brock TD, Madigan MT (1988) Biology of microorganisms, 5th edn. Prentice Hall, Englewood cliffs, NJ

    Google Scholar 

  • Broman D, Näuf C, Lundbergh I, Zebühr Y (1990) An in situ study on the distribution, biotransformation and flux of polycyclic aromatic hydrocarbons (pahs) in an aquatic food chain (seston‐Mytilus edulis L.‐Somateria mollissima L.) from the baltic: An ecotoxicological perspective. Environ Toxicol Chemi 9(4):429–442

    CAS  Google Scholar 

  • Buha A (2011) Polycyclic aromatic hydrocarbons. Toxipedia, 1:12–16.

  • Bustamante MA, Mier MV, Estrada JA, Domiguez CD (2011) Nitrogen and potassium variation on contaminant removal for a vertical subsurface flow lab scale constructed wetland. Bioresour Technol 102(17):7745–7754

    Article  CAS  Google Scholar 

  • Byeong-Kyu Lee (2010) Sources, distribution and toxicity of polyaromatic hydrocarbons (PAHs) in particulate matter, air pollution. Vanda Villanyi (ed), InTech, doi:10.5772/10045.

  • Calabrò V, Basile A (2011) Fundamental membrane processes science and engineering. In advanced membrane science and technology for sustainable energy and environmental applications. Basile A and Nunes SP (eds), Woodhead Publishing: Cambridge, UK and Italy, p 3–18

  • Cameotra SS, Bollaga J (2003) Biosurfactant-enhanced bioremediation of polycyclic aromatic hydrocarbons. Crit Rev Environ Sci Technol 33(2):111–126

    Article  CAS  Google Scholar 

  • Carls MG, Rice SD, Hose JE (1999) Sensitivity of fish embryos to weathered crude oil: Low level exposure during incubation causes malformations, genetic damage, and mortality in larval Pacific herring (Clupea pallasi). Environ Toxicol Chem 18:481–493

    Article  CAS  Google Scholar 

  • Castaldini F (2008) Bioremediation of PAHs- limitations and solutions. Universita Di Bologna Alma Mater Digital Library. Doctoral dissertation. Accessed 26 Jun 2013

  • Canadian Council of Ministers of the Environment (CCME) (1999). A protocol for the derivation of ecological effects-based and human health-based soil quality criteria for contaminated sites, Ottawa. CCME subcommittee on Environmental quality criteria for contaminated sites, Environment Canada

  • Canadian Council of Ministers of the Environment (CCME). 2008. Canadian Soil Quality Guidelines: Carcinogenic and Other Polycyclic Aromatic Hydrocarbons (PAHs) (Environmental and Human Health Effects). Canadian Council of Ministers of the Environment, Ottawa, Canada

  • Centers for Disease Control and Prevention (CDC) (2009) Fourth National Report on Human Exposure to Environmental Chemicals. Accessed 22 Aug 2014

  • Cerniglia CE (1992) Biodegradation of polycyclic aromatic hydrocarbons. Biodegradation 3:351–368

    Article  CAS  Google Scholar 

  • Chadrankant SK, Shwetha SR (2011) Role of microbial enzymes in the bioremediation of pollutants: A Review. Enzyme Res 11:1–11

    Google Scholar 

  • Chan SMN, Luan T, Wong MH (2006) Removal and biodegradation of polycyclic aromatic hydrocarbons by Selenastrum capricornutum. Environ Toxicol Chem 25(7):1772–1779

    Article  CAS  Google Scholar 

  • Chen YC, Banks MK, Schwab AP (2003) Pyrene degradation in the rhizosphere of tall fescue (Festuca arundinacea) and switchgrass (Panicum Virgatum). Environ Sci Technol 37:5778–5782

    Article  CAS  Google Scholar 

  • Choi J, Oris JT (2003) Assessment of the toxicity of anthracene photo-modification products using the topminnow (Poeciliopsis lucida) hepatoma cell line (PLHC-1). Aquat Toxicol 65(3):243–251

    Article  CAS  Google Scholar 

  • Choi H, Harrison R, Komulainen H, Delgado Saborit JM (2010) Polycyclic aromatic hydrocarbons. WHO Guidelines for Indoor Air Quality: Selected Pollutants. World Health Organization, Geneva, p 289–345

    Google Scholar 

  • Chung SY, Yettella RR, Kim JS, Kwon K, Kim MC, Min DB (2011) Effects of grilling and roasting on the levels of polycyclic aromatic hydrocarbons in beef and pork. Food Chem 129(4):1420–1426

    Article  CAS  Google Scholar 

  • Coates JD, Woodard J, Allen J, Philip P, Lovely DR (1997) Anaerobic degradation of polycyclic aromatic hydrocarbons and alkanes in petroleum-contaminated marine harbour sediments. Appl Environ Microbiol 63:3589–3593

    CAS  Google Scholar 

  • Cody TE, Radike MJ, Warshawsky D (1984) The phototoxicity of benzo(a)pyrene in the green alga Selenastrum capricornutum. Environ Res 35(1):122–132

    Article  CAS  Google Scholar 

  • Coover MP, Simms RC (1987) Haz WastePlease provide article title in the reference Coover and Simms (1987). Haz Mat 4:69–82

    CAS  Google Scholar 

  • Cornelissen G, Gustafsson Ö, Bucheli TD, Jonker MT, Koelmans AA, van Noort PC (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(18):6881–6895

    Article  CAS  Google Scholar 

  • Cottin NC, Merlin G (2007) Study of pyrene biodegradation capacity in two types of solid media. Sci Total Environ 380:116–123

    Article  CAS  Google Scholar 

  • Couch JA, Harshbarger JC (1985) Effects of carcinogenic agents on aquatic animals: An environmental and experimental overview. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev 3(1):63–105

    Google Scholar 

  • Das P, Mukherjee S, Sen R (2008) Improved bioavailability and biodegradation of a model poly aromatic hydrocarbon by a biosurfactant producing bacterium of marine origin. Chemosphere 72:1229–1234

    Article  CAS  Google Scholar 

  • Das N, Chandran P (2011) Microbial degradation of petroleum hydrocarbon contaminants: An overview. Biotechnol Res Int 941810:1–13

    Google Scholar 

  • Dash HR, Mangwani N, Chakraborty J, Kumari S, Das S (2013) Marine bacteria: potential candidates for enhanced bioremediation. Appl Microbiol Biotechnol 97:561–571

    Article  CAS  Google Scholar 

  • Decho AW (2000) Microbial biofilms in intertidal systems: An overview. Cont Shelf Res 20:1257–1273

    Article  Google Scholar 

  • Decker EL, Reski R (2008) Current achievements in the production of complex biopharmaceuticals with moss bioreactors. Bioprocess Biosyst Eng 31:3–9

    Article  CAS  Google Scholar 

  • Dennis MJ, Massey RC, McWeeny DJ, Knowles ME (1983) Analysis of polycyclic aromatic hydrocarbons in UK total diets. Fd Chem Toxic 21:569–574

    Article  CAS  Google Scholar 

  • Dennis MJ, Massey RC, Cripps G, Venn N, Howarth N, Lee G (1991) Factors affecting the polycyclic aromatic hydrocarbons content of cereals, fats and other food products. Food Addit Contam 8:517–530

    Article  CAS  Google Scholar 

  • de Vos RH, van Dokkum W, Schouten A, de Jong-Berkhout P (1990) Polycyclic aromatic hydrocarbons in Dutch total diet samples (1984–1986). Food Chem Toxicol 28(4):263–268

    Article  Google Scholar 

  • Ding J, Chen B, Zhu L (2013) Biosorption and biodegradation of polycyclic aromatic hydrocarbons by Phanerochaete chrysosporium in aqueous solution. Envir Chem 58(6):613–621

    CAS  Google Scholar 

  • Duedahl-Olesen L, White S, Binderup ML (2006) Polycyclic aromatic hydrocarbons (PAHs) in Danish smoked fish and meat products. Polycyclic Aromat Compd 26:163–164

    Article  CAS  Google Scholar 

  • Du W, Sun Y, Cao L, Huang J, Ji R, Wang X, Wu J, Zhu J, Guo H (2011) Environmental fate of phenanthrene in lysimeter planted with wheat and rice in rotation. J Hazard Mater 188:408–413

    Article  CAS  Google Scholar 

  • Dupraz C, Visscher PT (2005) Microbial lithification in marine stromatolites and hypersaline mats. Trends Microbiol 13(9):429–438

    Article  CAS  Google Scholar 

  • Dwivedi S (2012) Bioremediation of heavy metal by algae: current and future perspective. J Adv Lab Res Biol 3(3):195–199

    Google Scholar 

  • Environment Ontario (1992) Polycyclic Aromatic Hydrocarbons: sources, fate and levels in air, water, soil, sediments, sludge and food in Ontario. Report Number 0772992819, p 25–56. doi:10.5962/bhl.title.20226

  • Eisler R (2007) Polycyclic aromatic hydrocarbons In Eisler’s Encyclopedia of Environmentally Hazardous Priority Chemicals. Elsevier, The Netherlands, p 645–676

    Google Scholar 

  • Falahatpisheh MH, Donnelly KC, Ramos KS (2001) Antagonistic interactions among nephrotoxic polycyclic aromatic hydrocarbons. J Toxicol Environ Health 62(7):543–60

    Article  CAS  Google Scholar 

  • Farhadian A, Jinap S, Abas F, Sakar ZI (2010) Determination of polycyclic aromatic hydrocarbons in grilled meat. Food Control 21(5):606–610

    Article  CAS  Google Scholar 

  • Fernández-Luqueño F, Valenzuela-Encinas C, Marsch R, Martínez-Suárez C, Vázquez-Núñez E, Dendooven L (2011) Microbial communities to mitigate contamination of PAHs in soil—possibilities and challenges: a review. Environ Sci Pollut Res 18:12–30

    Article  CAS  Google Scholar 

  • Fismes J, Perrin-Ganier C, Empereur-Bissonnet P, Morel JL (2002) Soil-to-root transfer and translocation of polycyclic aromatic hydrocarbons by vegetables grown on industrial contaminated soil. J Environ Qual 31(5):1649–1656

    Article  CAS  Google Scholar 

  • Fulekar MH, Geetha M (2008) Bioremediation of chlorpyrifos in surface soil treatment unit using microbial consortium. Can J Pure Appl Sci 2(2):267–273

    Google Scholar 

  • Gan S, Lau EV, Ng HK (2009) Remediation of soils contaminated with polycyclic aromatic hydrocarbons (PAHs). J Hazard Mater 172(2–3):532–549

    Article  CAS  Google Scholar 

  • Garcia-Londoño VA, Garcia LP, Scussel VM (2013) Polycyclic aromatic hydrocarbons in milk powders marketed in Argentina and Brazil. Food Addit Contam 30(9):1573–1580

    Article  CAS  Google Scholar 

  • Geffard O, Geffard A, His E, Budzinski H (2003) Assessment of the bioavailability and toxicity of sediment-associated polycyclic aromatic hydrocarbons and heavy metals applied to Crassostrea gigas embryos and larvae. Mar Pollut Bull 46(4):481–490

    Article  CAS  Google Scholar 

  • Gentry TJ, Rensing C, Pepper IL (2004) New approaches for bioaugmentation as a remediation technology. Crit Rev Environ Sci Technol 34:447–494

    Article  CAS  Google Scholar 

  • Girellia AM, Speratia D, Tarolab AM (2014) Determination of polycyclic aromatic hydrocarbons in Italian milk by HPLC with fluorescence detection. Food Addit Contam Part A 31(4):703–710

    Article  CAS  Google Scholar 

  • Gomaa EA, Gray JI, Rabie S, Lopez-Bote C, Booren AM (1993) Polycyclic aromatic hydrocarbons in smoked food products and commercial liquid smoke flavourings. Food Addit Contam 10:503–521

    Article  CAS  Google Scholar 

  • Gomes A, Santos C, Almeida J, Elias M, Roseiro LC (2013) Effect of fat content, casing type and smoking procedures on PAHs contents of Portuguese traditional dry fermented sausages. Food Chem Toxicol 58:369–374

    Article  CAS  Google Scholar 

  • Grotte M, Schuurmann G, Altenburger R (2005) Modeling photo induced algae toxicity of polycyclic aromatic hydrocarbons. Environ Sci Technol 39:4141–4149

    Article  CAS  Google Scholar 

  • Guillen F, Gómez-Toribio V, Martı́nez MJ, Martı́nez AT (2000) Production of hydroxyl radical by the synergistic action of fungal laccase and aryl alcohol oxidase. Arch Biochem Biophys 383:142–147

    Article  CAS  Google Scholar 

  • Habe H, Omori T (2003) Genetics of polycyclic aromatic hydrocarbon metabolism in diverse aerobic bacteria. Biosci Biotechnol Biochem 67(2):225–243

    Article  CAS  Google Scholar 

  • Hajisamoh A (2013) Pollution Levels of 16 Priority PAHs in the major Rivers of Southern Thailand. J Chem 2(1):7–11

    CAS  Google Scholar 

  • Haritash AK, Kaushik CP (2009) Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): A review. J Hazard Mater 169(1):1–15

    Article  CAS  Google Scholar 

  • Harvey RG (1997) Polycyclic aromatic hydrocarbons: Chemistry and Carcinogenicity. In: Neilson AH (ed) Cambridge Monographs on Cancer Research. Wiley, New York, NY, pp 667–670

    Google Scholar 

  • Harvey RG (1998) Environmental chemistry of PAHs. In: Neilson AH (ed) The handbook of environmental chemistry: PAHs and related compounds. Springer, New York, NY, p 1–54

    Google Scholar 

  • Hatch AC, Burton GA (1999) Photo-induced toxicity of PAHs to Hyalella azteca and Chironomus tentans: effects of mixtures and behavior. Environ Pollut 106(2):157–167

    Article  CAS  Google Scholar 

  • Hatzinger PB, Alexander M (1995) Effect of aging on chemicals in soil on their biodegradability and extractability. Environ Sci Technol 29:537–545

    Article  CAS  Google Scholar 

  • Heijden SAVD, Jonker MT (2009) PAH bioavailability in field sediments: comparing different methods for predicting in situ bioaccumulation. Environ Sci Technol 43(10):3757–3763

    Article  CAS  Google Scholar 

  • Hellou J, Leonard J, Collier TK, Ariese F (2006) Assessing PAH exposure in feral finfish from the Northwest Atlantic. Mar Pollut Bull 52(4):433–441

    Article  CAS  Google Scholar 

  • Hjorth M, Vester J, Henriksen P, Forbes V, Dahllof I (2007) Functional and structural responses of marine planktonic food web to pyrene contamination. Mar Ecol Prog Ser 338:21–31

    Article  CAS  Google Scholar 

  • Hose JE, Brown ED (1998) Field applications of the piscine anaphase aberration test: lessons from the Exxon Valdez oil spill. Mutat Res 399:167–178

    Article  CAS  Google Scholar 

  • Howard PH, Meylan WM (1997) Handbbok of Physical Properties of Organic Chemicals. CRC Press, Inc, Boca Raton, FL, p 288

  • Husain A, Naeemi E, Dahsti B, Al-Omirah H, Al-Zenki S (1997) Polycyclic aromatic hydrocarbons in food products originating from locally reared animals in Kuwait. Food Addit Contam 14:295–299

    Article  CAS  Google Scholar 

  • Ikenaka Y, Sakamoto M, Nagata T, Takahashi H, Miyabara Y, Hanazato T, Ishizuka M, Isobe T, Kim JW, Chang KH (2013) Effects of polycyclic aromatic hydrocarbons (PAHs) on an aquatic ecosystem: acute toxicity and community level toxic impact tests of benzo(a)pyrene using lake zooplankton community. J Toxicol Sci 38(1):131–136

    Article  CAS  Google Scholar 

  • Inakollu S, Hung H, Shreve GS (2004) Biosurfactant enhancement of microbial degradation of various structural classes of hydrocarbon in mixed waste systems. Environ Eng Sci 21:463–469

    Article  CAS  Google Scholar 

  • International Programme on Chemical Safety (IPCS) (2000) Human exposure assessment; Environmental Health Criteria, 214. www.inchem.org/documents/ehc/214. Accessed 14 Feb 2014

  • International Union of Pure and Applied Chemistry (IUPAC) (2014) Compendium of Chemical Terminology, Gold book ‘Bioreactor’. 2nd edition, Version 2.33 p 166.

  • Ji X, Ripp SA, Layton AC, Sayler GS, De Bruyn JM (2013) Assessing long term effects of bioremediation: soil bacterial communities 14 years after polycyclic aromatic hydrocarbon contamination and introduction of a genetically engineered microorganism. J Bioremed Biodeg doi:10.4172/2155-6199.1000209

  • Johnsen A, Karlson U (2005) PAH degradation capacity of soil microbial communities: Does it depend on PAH exposure? Microb Ecol 50:488–495

    Article  CAS  Google Scholar 

  • Jones KC, Alcock RE, Johnson DL, Semple KT, Woolgar PJ (1996) Organic chemicals in contaminated land: analysis, significance and research priorities. Land Contam Reclamat 4(3):189–198

    Google Scholar 

  • 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 Biodegradation 45(1–2):57–88

    Article  CAS  Google Scholar 

  • Juckpecha K, Pinyakonga O, Rerngsamrana P (2012) Degradation of polycyclic aromatic hydrocarbons by newly isolated Curvularia sp. F18, Lentinus sp. S5 and Phanerochaete sp. T20. Sci Asia 38:147–156

    Article  CAS  Google Scholar 

  • Kaag NHBM, Foekema EM, Scholten MCTh, van Straalen NM (1997) Comparison of contaminant accumulation in three species of marine invertebrates with different feeding habits. Environ Toxicol Chem 16:837–842

    Article  CAS  Google Scholar 

  • Kamaljit B, Gurpal ST, Tait C, Lena M (2010) Polycyclic aromatic hydrocarbons in urban soils of different land uses in Miami, Florida. Soil Sediment Contam 19:231–243

    Article  CAS  Google Scholar 

  • Kanaly RA, Harayama S (2000) Biodegradation of High-Molecular-Weight Polycyclic Aromatic Hydrocarbons by Bacteria. J Bacteriol 182(8):2059–2067

    Article  CAS  Google Scholar 

  • Karigar CS, Rao SS (2011) Role of microbial enzymes in the bioremediation of pollutants: a Review. Enzyme Res 1:1–11

    Article  CAS  Google Scholar 

  • Karthikeyan R, Bhandari A (2001) Anaerobic biotransformation of aromatic and polycyclic aromatic hydrocarbons in soil microcosms: A review. J Hazard Subst Res 3:3–19

    Google Scholar 

  • Karyab H, Yunesian M, Nasseri S, Mahvi AH, Ahmadkhaniha R, Rastkari N, Nabizadeh R (2013) Polycyclic aromatic hydrocarbons in drinking water of Tehran, Iran. J Environ Health Sci Eng 11:25. doi: 10.1186/2052-336X-11-25

    Article  CAS  Google Scholar 

  • Kayal SI, Connell DW (1990) Partitioning of unsubstituted polycyclic aromatic hydrocarbons between surface sediments and the water column in the Brisbane river estuary. Mar Freshwater Res 41(4):443–456

    Article  CAS  Google Scholar 

  • Ke L, Luo L, Wang P, Luan T, Tam NF (2010) Effects of metals on biosorption and biodegradation of mixed polycyclic aromatic hydrocarbons by a freshwater green alga Selenastrum capricornutum. Bioresour Technol 101(18):6950–6961

    Article  CAS  Google Scholar 

  • Ke CL, Gu YG, Liu Q, Li LD, Huang HH, Cai N, Sun ZW (2017) Polycyclic aromatic hydrocarbons (PAHs) in wild marine organisms from South China Sea: Occurrence, sources, and human health implications. Mar Poll Bull doi:10.1016/j.marpolbul.2017.02.018

  • Kelly BC, Ikonomou MG, Blair JD, Morin AE, Gobas FA (2007) Food web–specific biomagnification of persistent organic pollutants. Science 317(5835):236–239

    Article  CAS  Google Scholar 

  • Kim SJ, Kweon O, Jones RC, Freeman JP, Edmondson RD, Cerniglia CE (2007) Complete and integrated pyrene degradation pathway in Mycobacterium vanbaalenii PYR-1 based on systems biology. J Bacteriol 189:464–472

    Article  CAS  Google Scholar 

  • Kim KH, Jahan SA, Kabir E, Brown RJC (2013) A review of airborne polycyclic aromatic hydrocarbons (PAHs) and their human health effects. Environ Int 60:71–80

    Article  CAS  Google Scholar 

  • Kishikawa N, Wada M, Kuroda N, Akiyama S, Nakashima N (2003) Determination of polycyclic aromatic hydrocarbons in milk sample by high-performance liquid chromatography with fluorescence detection. J Chromatogr Part B 789:257–264

    Article  CAS  Google Scholar 

  • Kostka JE, Prakash O, Overholt WA, Green SJ, Freyer G, Canion A et al. (2011) Hydrocarbon-degrading bacteria and the bacterial community response in gulf of Mexico beach sands impacted by the Deepwater Horizon oil spill. Appl Environ Microbiol 77:7962–7974

    Article  CAS  Google Scholar 

  • Kotterman MJJ, Rietberg HJ, Hage A, Field JA (1998) Polycyclic aromatic hydrocarbon oxidation by the white-rot fungus Bjerkandera sp. strain BOS55 in the presence of nonionic surfactants. Biotechnol Bioeng 57(2):220–227

    Article  CAS  Google Scholar 

  • Kuyukina MS, Ivshina IB, Makarov SO, Litvinenko LV, Cunningham CJ, Philip CJ (2005) Effect of biosurfactants on crude oil desorption and mobilization in a soil system. Environ Int 31:155–161

    Article  CAS  Google Scholar 

  • Kweon O, Kim SJ, Holland RD, Chen H, Kim DW, Gao Y, Yu LR, Baek S, Baek DH, Ahn H (2011) Polycyclic aromatic hydrocarbon metabolic network in Mycobacterium vanbaalenii PYR-1. J Bacteriol 193:4326–4337

    Article  CAS  Google Scholar 

  • Labana S, Kapur M, Malik DK, Prakash D, Jain RK (2007) Diversity, biodegradation and bioremediation of polycyclic aromatic hydrocarbons. In: Sing SN, Tripathi RD (eds) Environmental bioremediation technologies, Springer, Berlin, Heidelberg, p 409–443

  • Lampi MA, Gurska J, McDonald KI, Xie F, Huang XD, Dixon DG, Greenberg BM (2006) Photoinduced toxicity of polycyclic aromatic hydrocarbons to Daphnia magna: Ultraviolet‐mediated effects and the toxicity of polycyclic aromatic hydrocarbon photoproducts. Environ Toxicol Chem 25(4):1079–1087

    Article  CAS  Google Scholar 

  • Langenbach T (2013) Persistence and bioaccumulation of persistent organic pollutants (POPs). In: Yogesh B, Patil, Prakash R (eds) Agricultural and biological sciences; Applied bioremediation- active and passive approaches. Rijeka, Croatia, p 223–229

  • Latimer JS, Zheng J (2003) The sources, transport and fate of PAHs in the marine environment. In: Douben PE (ed) PAHs: An ecotoxicology perspective. Wiley, West Sussex, UK, p 9–33

    Google Scholar 

  • Lau KL, Tsang YY, Chiu SW (2003) Use of spent mushroom compost to bioremediate PAH-contaminated samples. Chemosphere 52:1539–1546

    Article  CAS  Google Scholar 

  • Ławniczak Ł, Marecik R, Chrzanowski Ł (2013) Contributions of biosurfactants to natural or induced bioremediation. Appl Microbiol Biotechnol 97(6):2327–2339

    Article  CAS  Google Scholar 

  • Lawrence JF, Weber DF (1984) Determination of polycyclic aromatic hydrocarbons in some Canadian commercial fish, shellfish, and meat products by liquid chromatography with confirmation by capillary gas chromatography-mass spectrometry. J Agric Food Chem 32:789–794

    Article  CAS  Google Scholar 

  • Layshock JA, Wilson G, Anderson KA (2010) Ketone and quinone‐substituted polycyclic aromatic hydrocarbons in mussel tissue, sediment, urban dust, and diesel particulate matrices. Environ Toxicol Chem 29(11):2450–2460

    Article  CAS  Google Scholar 

  • Lemon KP, Higgins DE, Kolter R (2007) Flagella-mediated motility is critical for Listeria monocytogenes biofilm formation. J Bacteriol 189:4418–4424

    Article  CAS  Google Scholar 

  • Lenicek J, Sekyra M, Pandey P, Citkova M, Be-Nes I, Novotna J, Kociano S, Helaskova J, Simonova A (1997) Polycyclic aromatic hydrocarbon at “program teplice” sites in the Czech Republic. Toxicol Environ Chem 58:25–35

    Article  CAS  Google Scholar 

  • Liang Y, Van Nostrand JD, Deng Y, He Z, Wu L, Zhang X, Li G, Zhou J (2011) Functional gene diversity of soil microbial communities from five oil-contaminated fields in China. ISME J 5:403–413

    Article  Google Scholar 

  • Liu J, Zhang L, Winteroth L, Garcia M, Weiman S, Wong J, Sunwoo J, Nadeou K (2013) Epigenetically mediated pathogenic effects of phenanthrene on regulatory T cells. J Toxicol 12:104–116

    Article  CAS  Google Scholar 

  • Lovley DR (2003) Cleaning up with genomics: applying molecular biology to bioremediation. Nat Rev Microbiol 1:35–44

    Article  CAS  Google Scholar 

  • Luch A (2005) The carcinogenic effects of polycyclic aromatic hydrocarbons. Imperial College Press, London, p 223–300. ISBN 1-86094-417-5

    Book  Google Scholar 

  • Lundestedt S (2003) Analysis of PAHs and their transformation products in contaminated soil and remedial processes. Dissertation, Umea University

  • Lundstedt S, White PA, Lemieux CL, Lynes KD, Lambert IB, Öberg L, Haglund P, Tysklind M (2007) Sources, fate, and toxic hazards of oxygenated polycyclic aromatic hydrocarbons (PAHs) at PAH-contaminated sites. AMBIO: A. J Human Environ 36(6):475–485

    Article  CAS  Google Scholar 

  • Luo L, Wang P, Lin L, Luan T, Ke L, Tam NF (2014) Removal and transformation of high molecular weight polycyclic aromatic hydrocarbons in water by live and dead microalgae. Process Biochem 49(10):1723–1732

    Article  CAS  Google Scholar 

  • Lu X, Reible DD, Fleeger JW (2006) Bioavailability of polycyclic aromatic hydrocarbons in field-contaminated Anacostia River (Washington, DC) sediment. Environ Toxicol Chem 25(11):2869–2874

    Article  CAS  Google Scholar 

  • Lu JC, Li ZT, Hussain K, Yang GK (2011) Bioremediation: The new directions of oil spill cleanup. Middle-East J Sci Res 7(5):738–740

    Google Scholar 

  • Mackay D, Fraser A (2000) Bioaccumulation of persistent organic chemicals: Mechanisms and models. Environ Pollut 110:375–391

    Article  CAS  Google Scholar 

  • Maier RM, Pepper IL, Gerba CP (2000) Environmental Microbiology. Academic Press, New York, NY, p 112–132

    Google Scholar 

  • Maier RM, Soberón-Chávez G (2000) Pseudomonas aeruginosa rhamnolipids: biosynthesis and potential applications. Appl Microbiol Biotechnol 54:625–633

    Article  CAS  Google Scholar 

  • Maisto G, De Nicola F, Iovieno P, Prati MV, Alfani A (2006) PAHs and trace elements in volcanic urban and natural soils. Geoderma 136:20–27

    Article  CAS  Google Scholar 

  • Makkar RS, Rockne KJ (2003) Comparison of synthetic surfactants and biosurfactants in enhancing biodegradation of polycyclic aromatic hydrocarbons. Environ Toxicol Chem 22(10):2280–2292

    Article  CAS  Google Scholar 

  • Maliszewska-Kordybach B (1999) Sources, concentrations, fate and effects of polycyclic aromatic hydrocarbons (PAHs) in the environment. Part A: PAHs in Air. Pol J Environ Stud 8(3):131–136

    CAS  Google Scholar 

  • Manoli E, Samara C (1999) Polycyclic aromatic hydrocarbons in natural waters: sources, occurrence and analysis. Trends Analyt Chem 18(6):417–428

    Article  CAS  Google Scholar 

  • Margesin R, Schinner F (2001a) Bioremediation (natural attenuation and biostimulation) of diesel-oil-contaminated soil in alpine glacier skiing area. Appl Environ Microbiol 67(7):3127–3133

    Article  CAS  Google Scholar 

  • Margesin R, Schinner F (2001b) Biodegradation and bioremediation of hydrocarbons in extreme environments. Appl Environ Microbiol 56:650–663

    CAS  Google Scholar 

  • Martineau D, Lemberger K, Dallaire A, Labelle P, Lipscomb T, Michel P, Mikaelian I (2002) Cancer in wildlife, a case study: Beluga from the St. Lawrence Estuary, Québec, Canada. Environ Health Perspect 110:285–292

    Article  Google Scholar 

  • Mascarelli A (2010) Deepwater horizon: After the oil. Nat News 467:22–24. doi:10.1038/467022a

    Article  CAS  Google Scholar 

  • Mastrangela G, Fadda E, Marzia V (1999) Polycyclic aromatic hydrocarbons and cancer in man. Environ Health Perspect 104:1166–1170

    Article  Google Scholar 

  • McElroy AE, Leitch K, Fay A (2000) A survey of in vivo benzo[a]pyrene metabolism in small benthic marine invertebrates. Mar Environ Res 50:33–38

    Article  CAS  Google Scholar 

  • McGrath TE, Chan WG, Hajaligol MR (2003) Low temperature mechanism for the formation of polycyclic aromatic hydrocarbons from the pyrolysis of cellulose. J Anal Appl Pyrol 66(1–2):51–70

    Article  CAS  Google Scholar 

  • Meador JP, Stein JE, Reichert WL, Varanasi U (1995) Bioaccumulation of polycyclic aromatic hydrocarbons by marine organisms. Rev Environ ContamToxicol 143:79–165

    CAS  Google Scholar 

  • Meador JP (2003) in Marine Invertebrates. PAHs: An ecotoxicological perspective, 147–171

  • Meador JP, Sommers FC, Ylitalo GM, Sloan CA (2006) Altered growth and related physiological responses in juvenile Chinook salmon (Oncorhynchus tshawytscha) from dietary exposure to polycyclic aromatic hydrocarbons (PAHs). Can J Fish Aquat Sci 63(10):2364–2376

    Article  CAS  Google Scholar 

  • Meador JP (2012) Polycyclic Aromatic Hydrocarbons. Reference module in earth systems and environmental sciences. Encyclopedia Ecol 2008:2881–2891

    Google Scholar 

  • Menichini E, Bocca B (2003) Em Encyclopedia of Food Sciences and Nutrition. In: Caballero B, Trugo LC, Finglas PM (eds) Encyclopaedia of food sciences and nutrition. Academic Press, Amsterdam, The Netherlands, p 4616

  • Minai TD, Minoui S, Hefatmanesh A (2012) Effect of salinity on biodegradation of polycyclic aromatic hydrocarbons (PAHs) of heavy crude oil in soil. Bull Environ Contam Toxicol 82:179–184

    Article  CAS  Google Scholar 

  • Motelay-Masseia A, Garban B, Tiphagne-larcher K, Chevreuil M, Ollivon D (2006) Mass balance for polycyclic aromatic hydrocarbons in the urban watershed of Le Havre (France): Transport and fate of PAHs from the atmosphere to the outlet. Water Res 40(10):3–11

    Google Scholar 

  • Mohan SV, 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

    Article  CAS  Google Scholar 

  • Morrison HA, Gobas FA, Lazar R, Haffner GD (1996) Development and verification of a bioaccumulation model for organic contaminants in benthic invertebrates. Environ Sci Technol 30(11):3377–3384

    Article  CAS  Google Scholar 

  • Mrozik A, Piotrowska-Seget Z, Labuzek S (2009) Bacterial degradation and bioremediation of polycyclic aromatic hydrocarbons. Pol J Environ Stud 12(1):15–25

    Google Scholar 

  • Muckian L, Grant R, Clipson N, Doyle E (2009) Bacterial community dynamics during bioremediation of phenanthrene and fluoranthene amended soil. Int Biodeterior Biodegradation 63:52–56

    Article  CAS  Google Scholar 

  • Mueller JG, Cerniglia CE, Pritchard PH (1996) Bioremediation of environments contaminated by polycyclic aromatic hydrocarbons. Biotechnology Research Series 6:125–194

    CAS  Google Scholar 

  • Mulder H, Breure AM, Van-Honschooten D, Grotenhuis JTC, Van-Andel JG, Rulkens WH (1998a) Effect of biofilm formation by Pseudomonas 8909N on the bioavailability of solid naphthalene. Appl Microbol Biotechnol 50:277–283

    Article  CAS  Google Scholar 

  • Mulder H, Breure AM, Van Andel JG, Grotenhuis JTC, Rulkens WH (1998b) Influence of hydrodynamic conditions on naphthalene dissolution and subsequent biodegradation. Biotechnol Bioeng 57:145–154

    Article  CAS  Google Scholar 

  • Müller R, Antranikian G, Maloney S, Sharp R (1998) Thermophilic degradation of environmental pollutants. In: Antranikian G (ed) Biotechnology of Extremophiles, (Advances in Biochemical Engineering/Biotechnology). Vol. 61, Springer, Berlin, Heidelberg, New York, p 155–169

    Chapter  Google Scholar 

  • Mulligan CN, Gibbs BF (2004) Types, production and applications of biosurfactant Products. Proc Indian Natn Sci Acad B70(1):31–55

    Google Scholar 

  • Narro ML, Cemiglia CE, Van Baalen C, Gibson DT (1992a) Evidence of NIH shift in naphthalene oxidation by the marine cyanobacterium, Osciiiatoria species strain JCM. Appl Environ Microbiol 58:1360–1363

    CAS  Google Scholar 

  • Narro ML, Cemiglia CE, Van Baalen C, Gibson DT (1992b) Metabolism of phenanthrene by the marine cyanobacterium Agmenellum quadruplicatum, strain PR-6. Appl Environ Microbiol 58:1351–1359

    CAS  Google Scholar 

  • Nedwell DB (1999) Effect of low temperature on microbial growth: lowered affinity for substrates limits growth at low temperature. FEMS Microbiol Ecol 30(2):101–111

    Article  CAS  Google Scholar 

  • New Jersey Department of Health and Senior Services (1999) Hazardous Substance Fact Sheet. CAS number 86-73-7

  • Nfon E, Cousins IT, Broman D (2008) Biomagnification of organic pollutants in benthic and pelagic marine food chains from the Baltic Sea. Sci Total Environ 397(1):190–204

    Article  CAS  Google Scholar 

  • Nguyen TT, Youssef NH, McInerney MJ, Sabatini DA (2008) Rhamnolipid biosurfactant mixtures for environmental remediation. Water Res 42:1735–1743

    Article  CAS  Google Scholar 

  • Nievas ML, Commendatore MG, Estevas JL, Bucalá V (2008) Biodegradation pattern of hydrocarbons from a fuel oil-type complex residue by an emulsifier-producing microbial consortium. J Hazard Mater 154:96–104

    Article  CAS  Google Scholar 

  • Nigam PS, Singh A (2011) Production of liquid biofuels from renewable resources. Prog Energy Combust Sci 37(1):52–68

    Article  CAS  Google Scholar 

  • Nkansah MA (2012) Environmental remediation: removal of polycyclic aromatic hydrocarbons. Dissertation, University of Bergen

  • Obayori OS, Ilori MO, Adebusoye SA, Oyetibo GO, Omotayo AE, Amund OO (2009) Degradation of hydrocarbons and biosurfactant production by Pseudomonas sp. strain LP1. World J Microbiol Biotechnol 25:1615–1623

    Article  CAS  Google Scholar 

  • Okere UV, Semple KT (2012) Biodegradation of PAHs in ‘pristine’ soils from different climatic regions. J Biorem Biodegrad 1(6):1–11

    Google Scholar 

  • Okoli CG, Ogbuagu DH, Madu GS, Njoku-Tony RF (2011) Proximal input of polynuclear aromatic hydrocarbons (PAHs) in groundwater sources of Okrika Mainland, Nigeria. Sci Res 2(6):848–854

    CAS  Google Scholar 

  • Olaniran AO, Balgobind A, Pillay B (2013) Bioavailability of heavy metals in soil: Impact on microbial biodegradation of organic compounds and possible improvement strategies. Int J Mol Sci 14(5):197–228

    Article  CAS  Google Scholar 

  • Olatunji OS, Fatoki OS, Opeolu BO, Xhimba BJ (2014) Determination of polycyclic aromatic hydrocarbons (PAHs) in processed meat products using gas chromatography – Flame ionization detector. Food Chem 156:296–300

    Article  CAS  Google Scholar 

  • Oris JT, Giesy JP (1985) The photoenhanced toxicity of anthracene to juvenile sunfish (Lepomis spp). Aquat Toxicol 6:133–146

    Article  CAS  Google Scholar 

  • Pacwa-Plociniczak M, Plaza GA, Piotrowska-Seget Z, Cameotra SS (2011) Environmental applications of biosurfactants: Recent advances. Int J Mol Sci 12(1):633–654

    Article  CAS  Google Scholar 

  • Pan E, Sun H, Xu Q,Zhang Q, Liu LF, Chen XD, Xu Y (2015) Polycyclic aromatic hydrocarbons concentrations in drinking water in villages along the Huai River in China and their association with high cancer incidence in local population. BioMed Res Int Article ID 762832, doi:10.1155/2015/762832

  • Panalaks T (1976) Determination and identification of polycyclic aromatic hydrocarbons in smoked and charcoal-broiled food products by high pressure liquid chromatography and gas chromatography. J Environ Sci Health B 11:299–315

    Article  CAS  Google Scholar 

  • Pantsyrnayaa T, Blancharda F, Delaunaya S, Goergena JL, Guédona E, Gusevab E, Boudrant J (2011) Effect of surfactants, dispersion and temperature on solubility and biodegradation of phenanthrene in aqueous media. Chemosphere 83(1):29–33

    Article  CAS  Google Scholar 

  • Patel MS, Tiwari KK (2015) Remediation of Acenaphthene and Fluoranthene by Chlorella vulgaris Beijerinck: FTIR based study. Int J Biosci Technol 8(2):5–9

    Google Scholar 

  • Paul D, Pandey G, Pandey J, Jain RK (2005) Accessing microbial diversity for bioremediation and environmental restoration. Trends Biotechnol 23:135–142

    Article  CAS  Google Scholar 

  • Payne JF, Mathieu A, Collier TK (2003) Ecotoxicological studies focusing on marine and freshwater fish. In: Dauben PET (ed) PAHs-an ecotoxicological perspective. Wiley: West Sussex, UK, p 191–224

  • Pazos M, Rosales E, Alcántara T, Gómez J, Sanromán MA (2010) Decontamination of soils containing PAHs by electroremediation: a review. J Hazard Mater 177(1):1–11

    Article  CAS  Google Scholar 

  • Peng RH, Xiong AS, Xue Y, Fu XY, Gao F, Zhao W, Tian YS, Yao QH (2008) Microbial biodegradation of polyaromatic hydrocarbons. FEMS Microbiol Rev 32:927–955

    Article  CAS  Google Scholar 

  • Perelo LW (2010) Review: In situ and bioremediation of organic pollutants in aquatic sediments. J Hazard Mater 177(1–3):81–89

    Article  CAS  Google Scholar 

  • Perugini M, Visciano P, Giammarino A, Manera M, Di Nardo W, Amorena M (2007) Polycyclic aromatic hydrocarbons in marine organisms from the Adriatic Sea, Italy. Chemosphere 66:1904–1910

    Article  CAS  Google Scholar 

  • Petersen DG, Reichenberg F, Dahllof I (2008) Phototoxicity of pyrene affects benthic algae and bacteria from the Arctic. Environ Sci Technol 42:1371–1376

    Article  CAS  Google Scholar 

  • Petrun AC, Rubenchik BL (1966) On the possibility of appearance of the carcinogenous agent 3,4 benzpyrene in electrically smoked fish. Vrazhednoe Delo 2:93–95

    Google Scholar 

  • Pittinger CA, Buikema AL, Falkinham JO (1987) In-situ variations in oyster mutagenicity and tissue concentrations of polycyclic aromatic hydrocarbons. Environ Toxicol Chem 6:51–60

    CAS  Google Scholar 

  • Pollard SJT, Hrudey SE, Fedorak PM (1994) Bioremediation of petroleum and creosote-contaminated soils: A review of constraints. Waste Manag Res 12:173–194

    Article  CAS  Google Scholar 

  • Pozdnyakova NN (2012) Involvement of the ligninolytic system of white-rot and litter-decomposing fungi in the degradation of polycyclic aromatic hydrocarbons. Biotechnol Res Int 243217. doi:10.1155/2012/243217

  • Prabhu Y, Phale PS (2003) Biodegradation of Phenanthrene by Pseudomonas sp. Strain PP2: novel metabolic pathway role of biosurfactant and cell surface hydrophobicity in Hydrocarbon assimilation. Appl Microbiol Biotechnol 61:342–351

    Article  CAS  Google Scholar 

  • Pradhan SP, Conrad JR, Paterek JR, Srivastava VJ (1998) Potential of phytoremediation for treatment of PAHs in soil at MGP sites. J Soil Contam 7:467–480

    Article  CAS  Google Scholar 

  • Prince RC (2010) Bioremediation of marine oil spills. Handbook Hydrocarbon Lipid Microbiol 6:2617–2630

    Article  Google Scholar 

  • Purwaningsih IS, Hill GA, Headley JV (2002) Air stripping and dissolution rates of aromatic hydrocarbon particles in a bioreactor. Chem Eng Commun 189(2):268–283

    Article  CAS  Google Scholar 

  • Quinn L, Pieters R, Nieuwoudt C, Borgen A, Kylin H, Bouwman H (2009) Distribution profiles of selected organic pollutants in soils and sediments of industrial, residential and agricultural areas of South Africa. J Environ Monit 9(11):1647–1657

    Article  CAS  Google Scholar 

  • Rahman KSM, Rahman TJ, Lakshmanaperumalsamy P, Marchant R, Banat IM (2003) The potential of bacterial isolates for emulsification with range of hydrocarbons. Acta Biotechnol 4:335–345

    Article  Google Scholar 

  • Ramesh A, Walker SA, Hood DB, Guillien MD, Schneider K, Weyhand EH (2004) Bioavailability and risk assessment of orally ingested polycyclic aromatic hydrocarbons. Int J Toxicol 23(5):301–333

    Article  CAS  Google Scholar 

  • Reddy MS, Naresh B, Leela T, Prashanthi M, Madhusudhan NC, Dhanasri G, Devi P (2010) Biodegradation of phenanthrene with biosurfactant production by a new strain of Brevibacillus species. Bioresour Technol 101:7980–7983

    Article  CAS  Google Scholar 

  • Rehmann K, Noll HP, Steiberg CEW (1998) Pyrene degradation by Mycobacterium sp. Strain KR2. Chemosphere 6(14):2977–2992

    Article  Google Scholar 

  • Ren G, Ren W, Teng Y, Li Z (2015) Evident bacterial community changes but only slight degradation when polluted with pyrene in a red soil. Front Microbiol 6:22–33

    Google Scholar 

  • Rengarajana T, Rajendran P, Nandakumar N, Lokeshkumar B, Rajendran P, Nishigaki I (2015) Exposure to polycyclic aromatic hydrocarbons with special focus on cancer. Asian Pac J Trop Biomed 5(3):182–189

    Article  Google Scholar 

  • Rey-Salgueiro L, García-Falcón MS, Martínez-Carballo E, Simal-Gándara J (2008) Effects of toasting procedures on the levels of polycyclic aromatic hydrocarbons in toasted bread. Food Chem 108(2):607–615

    Article  CAS  Google Scholar 

  • Rey-Salgueiro L, Martínez-Carballo E, García-Falcón MS, Simal-Gándara J (2009) Occurrence of polycyclic aromatic hydrocarbons and their hydroxylated metabolites in infant foods. Food Chem 115:814–819

    Article  CAS  Google Scholar 

  • Rhodes A, Carlin A, Semple T (2008) Impact of black carbon in the extraction and mineralisation of phenanthrene in soil. Environ Sci Technol 42(3):740–745

    Article  CAS  Google Scholar 

  • Rice JW, Suuberg EM (2010) Thermodynamic study of (anthracene + benzo[a]pyrene) solid mixtures. J Chem Thermodyn 42(11):1356–1360

    Article  CAS  Google Scholar 

  • Riess R, Nemati M, Headley J, Hill G (2005) Improved mass transfer and biodegradation rates of naphthalene particles using a novel bead mill bioreactor. J Chem Technol Biotechnol 80(6):662–668

    Article  CAS  Google Scholar 

  • Robles-González IV, Fava F, Poggi-Varaldo HM (2008) A review on slurry bioreactors for bioremediation of soils and sediments. Microb Cell Fact 7:5–15

    Article  CAS  Google Scholar 

  • Roseiro LC, Gomes A, Santos C (2011) Influence of processing in the prevalence of polycyclic aromatic hydrocarbons in a Portuguese traditional meat products. Food Chem Toxicol 49:1340–1345

    Article  CAS  Google Scholar 

  • Romero MC, Cazau MC, Giorgieri S, Arambari AM (1998) Phenanthrene degradation by microorganisms isolated from a contaminated stream. Environ Pollut 101:335–359

    Article  Google Scholar 

  • Ruby MV, Lowney YW, Bunge AL, Roberts SM, Gomez-Eyles JL, Ghosh U, Kissel JC, Tomlinson P, Menzie C (2016) Oral Bioavailability, Bioaccessibility, and Dermal Absorption of PAHs from Soil—State of the Science. Environ Sci Technol 50(5):2151–2164

    Article  CAS  Google Scholar 

  • Samanta SK, Singh OV, Jain RK (2002) Polycyclic aromatic hydrocarbons: environmental pollution and bioremediation. Trends Biotechnol 20(6):243–248

    Article  CAS  Google Scholar 

  • Sanagi MM, Loh SH, Wan-Ibrahim WA, Hasan MH, Aboul-Enein HY (2013) Determination of polycyclic aromatic hydrocarbons in fresh milk by hollow fiber liquid-phase microextraction-gas chromatography mass spectrometry. J Chromatogr Sci 51:112–116

    Article  CAS  Google Scholar 

  • Schneegurt MA, Kulpa CF (1998) The application of molecular techniques in environmental biotechnology for monitoring microbial systems. Biotechnol Appl Biochem 27(2):73–79

    Article  CAS  Google Scholar 

  • Scientific Committee on Food, European Commission (2002) Opinion of the Scientific Committee on Food on the risks to human health of polycyclic aromatic hydrocarbons in food. http://ec.europa.eu/food/fs/sc/scf/out153_en.pdf. Accessed 15 May 2013

  • Semple KT, Cain RB, Schimdt S (1999) Biodegradation of aromatic compounds by microalgae. FEMS Microbiol Lett 170:291–300

    Article  CAS  Google Scholar 

  • Seo J, Young SK, Qing XL (2009) Bacterial degradation of aromatic compounds. Int J Environ Res Public Health 6(1):278–309

    Article  CAS  Google Scholar 

  • Sharma S (2012) Bioremediation: Features, Strategies and applications. Asian J Pharm Life Sci 2(2):202–213

    Google Scholar 

  • Shi W, Krella A, Orth A, Yu Y, Fundele R (2005) Widespread disruption of genomic imprinting in adult interspecies mouse (Mus) hybrids. Genesis 43(3):100–8

    Article  CAS  Google Scholar 

  • Shiraishi N, Pilkington NH, Otsuki A, Fuwa K (1985) Occurrence of chlorinated polynuclear aromatic hydrocarbons in tap water. Environ Sci Technol 19:585–590

    Article  CAS  Google Scholar 

  • Silva IS, Grossman M, Durranta LR (2009) Degradation of polycyclic aromatic hydrocarbons (2-7 rings) under microaerobic and very-low-oxygen conditions by soil fungi. Int Biodeter Biodegr 63(2):224–229

    Article  CAS  Google Scholar 

  • Silva BO, Adetunde OT, Oluseyi TO, Olayinka KO, Alo BI (2011) Effects of the methods of smoking on the levels of polycyclic aromatic hydrocarbons (PAHs) in some locally consumed fishes in Nigeria. African. J Food Sci 5(7):384–391

    CAS  Google Scholar 

  • Simon R, Gomez-Ruiz JA, Wenzi T (2010) Results of an European inter-laboratory comparison study on the determination of the 15+1 EU priority polycyclic aromatic hydrocarbons (PAHs) in liquid smoke condesates. Food Chem 123:819–826

    Article  CAS  Google Scholar 

  • Singh R, Paul D, Jain RK (2006) Biofilms: implications in bioremediation. Trends Microbiol 14(9):389–397

    Article  CAS  Google Scholar 

  • Siron R, Pelletier E, Brochu H (1995) Environmental factors influencing the biodegradation of petroleum hydrocarbons in cold seawater. Arch Environ Contam Toxicol 28:406–416

    Article  CAS  Google Scholar 

  • Skupinska K, Mislewicz I, Kasprzycka-Guttman T (2004) Polycyclic aromatic hydrocarbons: environmental appearance and impact on living organisms. Acta Pol Pharm 61(3):233–240

    CAS  Google Scholar 

  • Sojinu OS, Sonibare OO, Zeng EY (2011) Concentrations of polycyclic aromatic hydrocarbons in soils of a mangrove forest affected by a forest fire. Toxicol Environ Chem 93(3):450–461

    Article  CAS  Google Scholar 

  • Sowa D (2011) Sphingomonas spp: Agents of Bioremediation and Pathogenesis. From Microbe wiki, the student-edited microbiology resource. https://microbewiki.kenyon.edu. Accessed 27 July 2014

  • Sram RJ, Binková B, Rössner P, Rubeš J, Topinka J, Dejmeka J (1999) Adverse reproductive outcomes from exposure to environmental mutagens. Mutat Res 428:203–215

    Article  CAS  Google Scholar 

  • Srogi K (2007) Monitoring of environmental exposure to polycyclic aromatic hydrocarbons: a review. Environ Chem Lett 5(4):169–195

    Article  CAS  Google Scholar 

  • Storelli MM, Stuffler RG, Marcotrigiano GO (2003) Polycyclic aromatic hydrocarbons, polychlorinated biphenyls, chlorinated pesticides (DDTs), hexachlorocyclohexane, and hexachlorobenzene residues in smoked seafood. J Food Prot 66(6):1095–1099

    Article  CAS  Google Scholar 

  • Stumpe-Vīksna I, Bartkevičs V, Kukāre A, Morozovsa A (2008) Polycyclic aromatic hydrocarbons in meat smoked with different types of wood. Food Chem 110(3):794–797

    Article  CAS  Google Scholar 

  • Sudip KS, Om VS, Rakesh KJ (2002) Polycyclic aromatic hydrocarbons: environmental pollution and bioremediation. Trends Biotechnol 20:243–248

    Article  Google Scholar 

  • Sun RX, Lin Q, Ke CL, Du FY, Gu YG, Cao K, Xiao JL, Mai BX (2016) Polycyclic aromatic hydrocarbons in surface sediments and marine organisms from the Daya Bay, South China. Mar Poll Bull 103(1):325–332

    Article  CAS  Google Scholar 

  • Swaranjit SC, Randhir SM (2010) Biosurfactant-enhanced bioremediation of hydrophobic pollutants. Pure Appl Chem 82(1):97–116

    Google Scholar 

  • Takeuchi I, Miyoshi N, Mizukawa K, Takada H, Ikemoto T, Omori K, Tsuchiya K (2009) Biomagnification profiles of polycyclic aromatic hydrocarbons, alkylphenols and polychlorinated biphenyls in Tokyo Bay elucidated by δ 13 C and δ 15 N isotope ratios as guides to trophic web structure. Mar Poll Bull 58(5):663–671

    Article  CAS  Google Scholar 

  • Tam NFY, Chan MN, Wong YS (2010) Removal and biodegradation of polycyclic aromatic hydrocarbons by immobilized microalgal beads. Trans Ecol Environ, Waste Manag Environ 140:391–402. doi:10.2495/WM100351

    CAS  Google Scholar 

  • Tang Y, Qi JL, Krieger-Brockett B (2005) Evaluating factors that influence microbial phenanthrene biodegradation rates by regression with categorical variables. Chemosphere 59:729–741

    Article  CAS  Google Scholar 

  • Tekere M, Read J, Mattiasson B (2005) Polycyclic aromatic hydrocarbon biodegradation in extracellular fluids and static batch cultures of selected sub-tropical white rot fungi. J Biotechnol 115:367–77

    Article  CAS  Google Scholar 

  • Thomson B, Lake R, Lill R (1996) The contribution of margarine to cancer risk from polycyclic aromatic hydrocarbons in the New Zealand diet. Polycycl Aromat Compd 11:177–184

    Article  CAS  Google Scholar 

  • Ukiwe LN, Egereonu UU, Njoku PC, Nwoko CIA, Jude I, Allinor JI (2013) Polycyclic aromatic hydrocarbons degradation techniques: A review. Int J Chem 5(4):43–55

    Article  CAS  Google Scholar 

  • Valentı´n L, Nousiainen A, Mikkonen A (2013) Introduction to organic contaminants in soil: concepts and risks. In: Vincent T, Caminal G, Eljarrat E, Barceló D (eds) Emerging organic contaminants in sludges: analysis, fate and biological treatment. Springer-Verlag Berlin, Heidelberg 24: 1–30

  • Vandermeersch G, Lourenço HM, Alvarez-Muñoz D, Cunha S, Diogène J, Cano-Sancho G, Sloth JJ, Kwadijk C, Barcelo D, Allegaert W, Bekaert K (2015) Environmental contaminants of emerging concern in seafood–European database on contaminant levels. Environ Res 143:29–45

    Article  CAS  Google Scholar 

  • Van der Oost R, Beyer J, Vermeulen NP (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13(2):57–149

    Article  Google Scholar 

  • Varanasi U, Reichert WL, Stein JE (1989) 32P-Postlabeling analysis of DNA adducts in liver of wild English sole (Parophrys vetulus) and winter flounder (Pseudopleuronectes americanus). Cancer Res 49:11–71

    Google Scholar 

  • Vega S, Gutierrez R, Ortiz R, Schettino B, Ramirez M, Perez J (2011) Hydrocarbons derived from petroleum in bottled drinking water from Mexico city. Bull Environ Contam Toxicol 86:632–636

    Article  CAS  Google Scholar 

  • Venosa AD, Zhu X (2003) Biodegradation of crude oil contaminating marine shorelines and freshwater wetlands. Spill Sci Technol Bull 8(2):163–178

    Article  CAS  Google Scholar 

  • Vidali M (2001) Bioremediation: An overview. Pure Appl Chem 73(7):1163–1172

    Article  CAS  Google Scholar 

  • Viegas O, Novo P, Pinto E, Pinho O, Ferreira IMPLVO (2012) Effect of charcoal types and grilling conditions on formation of heterocyclic aromatic amines (HAs) and polycyclic aromatic hydrocarbons (PAHs) in grilled muscle foods. Food Chem Toxicol 50(6):2128–2134

    Article  CAS  Google Scholar 

  • Viñas M, Sabate J, Espuny M, Solanas A (2005) Bacterial community dynamics and polycyclic aromatic hydrocarbon degradation during bioremediation of heavily creosote contaminated soil. Appl Environ Microbiol 71(11):7008–7018

    Article  CAS  Google Scholar 

  • Volkering F, Breure AM, Van Andel JG (1993) Effect of microorganisms on the bioavailability and biodegradation of crystalline naphthalene. Appl Microbiol Biotechnol 40:535–540

    Article  CAS  Google Scholar 

  • Wan Y, Jin X, Hu J, Jin F (2007) Trophic dilution of polycyclic aromatic hydrocarbons (PAHs) in a marine food web from Bohai Bay, North China. Environ Sci Technol 41(9):3109–3114

    Article  CAS  Google Scholar 

  • Wang X, Brusseau ML (1993) Solubilisation of some low polarity organic compounds by hydroxypropyl-β-cyclodextrin. Environ Sci Technol 27:2821–2825

    Article  CAS  Google Scholar 

  • Wang G, Zhang Q, Ma P, Rowden J (2008) Sources and distribution of polycyclic aromatic hydrocarbons in urban soils. Case studies of Detroit and New Orleans. Soil Sediment Contam 17(6):547–563

    Article  CAS  Google Scholar 

  • Ward DM, Brock TD (1978) Hydrocarbon biodegradation in hypersaline environments. Appl Environ Microbiol 35:353–359

    CAS  Google Scholar 

  • Warshawsky D, Radike M, Jayasimhulu K, Cody T (1988) Metabolism of benzo(a)pyrene by a dioxygenase enzyme system of the freshwater alga Selenastrum capricornutum. Biochem Biophys Res Commun 152:540–544

    Article  CAS  Google Scholar 

  • Warshawsky D, Cody T, Radike M, Reilman R, Schumann B, LaDow K, Schneider J (1995) Biotransformation of benzo(a)pyrene and other polycyclic aromatic hydrocarbons and heterocyclic analogs by several green algae and other algal species under gold and white light. Chem Biol Interact 97:131–148

    Article  CAS  Google Scholar 

  • Warshawsky D, LaDow K, Schneider J (2007) Enhanced degradation of benzo[a]pyrene by Mycobacterium sp. in conjunction with green alga. Chemosphere 69(3):500–506

    Article  CAS  Google Scholar 

  • Web (2011) About coal tar and polycyclic aromatic hydrocarbons (PAHs). The truth about refined coal tar based pavement sealers and PAHs. http://www.truthaboutcoaltar.com/aboutcoaltar.html. Accessed 15 Oct 2014

  • Weeks BA, Warimer JE (1984) Effects of toxic chemicals on macrophage phagocytosis in two estuarine fishes. Mar Environ Res 14:327–335

    Article  CAS  Google Scholar 

  • Weis LM, Rummel AM, Masten SJ, Trosko JE, Upham BL (1998) Bay or bay like regions of polycyclic aromatic hydrocarbons were potent inhibitors of gap junctional intercellular communication. Environ Health Perspect 106(1):17–22

    Article  CAS  Google Scholar 

  • White PA, Robitaille S, Rasmussen JB (1999) Heritable reproductive effects of benzo(a)pyrene on the fathead minnow (Pimephales promelas). Environ Toxicol Chem 18:1843–1847

    Article  CAS  Google Scholar 

  • Wick AF, Haus NW, Sukkariyah BF, Haering KC, Daniels WL (2011) Remediation of PAH-contaminated soils and sediments: A literature review. CSES Department, Internal Research Document. p 1–102

  • Wilcke W (2000) Polycyclic aromatic hydrocarbons (PAHs) in soil. J Plant Nutr Soil Sci 163:229–248

    Article  CAS  Google Scholar 

  • Wild SR, Jones KC (1995) Polynuclear aromatic hydrocarbons in the United Kingdom environment: a preliminary source inventory and budget. Environ Pollut 88(1):91–108

    Article  CAS  Google Scholar 

  • Wilson SC, Jones KC (1993) Bioremediation of soil contaminated with polynuclear aromatic hydrocarbons (PAHs): A review. Environ Pollut 81(3):229–249

    Article  CAS  Google Scholar 

  • World Health Organisation (WHO) (2003). Polynuclear aromatic hydrocarbons in Drinking-water Background document for development of WHO Guidelines for Drinking-water Quality. p 4

  • Wu M, Chen L, Tian Y, Dinga Y, Dick WA (2013) Degradation of polycyclic aromatic hydrocarbons by microbial consortia enriched from three soils using two different culture media. Environ Pollut 178:152–158

    Article  CAS  Google Scholar 

  • Yakan SD, Focks A, Klasmeier J, Okay OS (2017) Numerical evaluation of bioaccumulation and depuration kinetics of PAHs in Mytilus galloprovincialis. Environ Pollut 220:1244–1250

    Article  CAS  Google Scholar 

  • Yang C, Zhang G, Wang Z, Yang Z, Hollebone B, Landriault M, Shah K, Brown CE (2014) Development of a methodology for accurate quantitation of alkylated polycyclic aromatic hydrocarbons in petroleum and oil contaminated environmental samples. Anal Methods 6(19):7760–7771

    Article  CAS  Google Scholar 

  • Yalkowsky SH, Dannenfelser RM (1992) The aquasol database of aqueous solubility, 5th edn. Univ Az, College of Pharmacy, Tucson, AZ

    Google Scholar 

  • Yanyangwu D (2012) Anaerobic biodegradation of PAHs in river sediments under denitrifying conditions-Another choice? Yanyangwu.wordpress.com. Accessed 4 Oct 2013

  • Zanieri L, Galvan P, Checchini L, Cincinelli A, Lepri L, Donzelli GP, Del Bubba M (2007) Polycyclic aromatic hydrocarbons (PAHs) in human milk from Italian women: Influence of cigarette smoke and residential area. Chemosphere 67:1265–1274

    Article  CAS  Google Scholar 

  • Zhang Y, Tao S (2009) Global atmospheric emission inventory of polycyclic aromatic hydrocarbons (PAHs) for 2004. Atmos Environ 43:812–819

    Article  CAS  Google Scholar 

  • Zhang J, Zhang X, Liu J, Li R, Shen B (2012) Isolation of a thermophilic bacterium, Geobacillus sp. SH-1, capable of degrading aliphatic hydrocarbons and naphthalene simultaneously, and identification of its naphthalene degrading pathway. Bioresour Technol 124:83–89

    Article  CAS  Google Scholar 

  • Zhou Q, Zhang J, Fu J, Shi J, Jiang G (2008) Biomonitoring: an appealing tool for assessment of metal pollution in the aquatic ecosystem. Anal Chim Acta 606:135e150

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors wish to acknowledge the financial support of the National Research Foundation (NRF), South Africa, through the Thuthuka Research Grant No. 84185 awarded to Prof B.O. Opeolu.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Oluwadara Oluwaseun Alegbeleye.

Ethics declarations

Conflict of Interest

The authors declare that they have no competing interests.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alegbeleye, O.O., Opeolu, B.O. & Jackson, V.A. Polycyclic Aromatic Hydrocarbons: A Critical Review of Environmental Occurrence and Bioremediation. Environmental Management 60, 758–783 (2017). https://doi.org/10.1007/s00267-017-0896-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00267-017-0896-2

Keywords

Navigation