A review of the bioaccumulation and adverse effects of PFAS in free-living organisms from contaminated sites nearby fluorochemical production plants

Abstract

Per- and polyfluoroalkyl substances (PFAS) encompass a large, heterogeneous group of chemicals of potential concern to human and environmental health. Based on information for some legacy PFAS, such as perfluorooctane sulfonate and perfluorooctanoate, there is an increasing awareness that they can represent a serious environmental risk. Although the environmental occurrence and fate of some legacy PFAS and their toxicity under controlled laboratory conditions have been investigated, to date, there is a dearth of information on the exposure and potential adverse effects of these compounds towards free-living organisms. The present review summarizes the findings of field studies investigating the accumulation and adverse effects induced by the exposure to environmental mixtures of both legacy and emerging PFAS in the wildlife living nearby fluorochemical production plants (FCP). Biomonitoring campaigns performed close to FCP, which can be considered as hotspots of PFAS contamination, can be very useful in exploring the fate and toxicity of these compounds towards free-living organisms. All studies showed that the bioaccumulation of both legacy and emerging PFAS in wildlife living near the FCP is higher compared to control sites and other areas worldwide. However, the investigation on adverse effects returned contrasting results, suggesting the need for further studies to shed light on the toxicity and mechanism(s) of action of PFAS in free-living organisms.

Keywords

Polyfluoroalkyl substances / ecotoxicology / toxic effects / free-living organisms / contaminated sites

References

[1] Kissa E. Fluorinated surfactants and repellents (Vol. 97); 2001. New York: Marcel Dekker, Inc.

[2] Moody CA.Perfluorinated surfactants and the environmental implications of their use in fire-fighting foams.Environ Sci Technol2000;34:3864-70

[3] Lanza HA,Mudge JF.Temporal monitoring of perfluorooctane sulfonate accumulation in aquatic biota downstream of historical aqueous film forming foam use areas.Environ Toxicol Chem2017;36:2022-9

[4] de Vries P,Kwadijk CJAF.The toxic exposure of flamingos to per- and Polyfluoroalkyl substances (PFAS) from firefighting foam applications in Bonaire.Mar Pollut Bull2017;124:102-11

[5] Navarro I,Sanz P.Uptake of perfluoroalkyl substances and halogenated flame retardants by crop plants grown in biosolids-amended soils.Environ Res2017;152:199-206

[6] Evich MG,McCord JP.Per- and polyfluoroalkyl substances in the environment.Science2022;375:eabg9065 PMCID:PMC8902460

[7] Wickham GM.Emerging contaminants, coerced ignorance and environmental health concerns: the case of per- and polyfluoroalkyl substances (PFAS).Sociol Health Illn2021;43:764-78

[8] Washington JW,McCord JP.Nontargeted mass-spectral detection of chloroperfluoropolyether carboxylates in New Jersey soils.Science2020;368:1103-7 PMCID:PMC7814412

[9] Wagner WE.Legal obstacles to toxic chemical research.Science2022;375:138-41

[10] Ankley GT,Hoke RA.Assessing the ecological risks of per- and polyfluoroalkyl substances: current state-of-the science and a proposed path forward.Environ Toxicol Chem2021;40:564-605 PMCID:PMC7984443

[11] Lindstrom AB,Libelo EL.Polyfluorinated compounds: past, present, and future.Environ Sci Technol2011;45:7954-61

[12] Jia S,Li C.Recent advances in mass spectrometry analytical techniques for per- and polyfluoroalkyl substances (PFAS).Anal Bioanal Chem2022;414:2795-807

[13] Glüge J,Cousins IT.An overview of the uses of per- and polyfluoroalkyl substances (PFAS).Environ Sci Process Impacts2020;22:2345-73 PMCID:PMC7784712

[14] ARPAV; 2019. Agenzia Regionale per la Prevenzione e Protezione Ambientale del Veneto. Il composto cC6O4 nel Po.

[15] ARPAV; 2020. Agenzia Regionale per la Prevenzione e Protezione Ambientale del Veneto. Sostanze perfluoro alchiliche (PFAS).

[16] Morganti M,Pascariello S.Exposure assessment of PFAS-contaminated sites using avian eggs as a biomonitoring tool: a frame of reference and a case study in the Po River valley (Northern Italy).Integr Environ Assess Manag2021;17:733-45

[17] ECHA; 2019. European chemicals agency: difluoro{[2,2,4,5-tetrafluoro-5-(trifluoromethoxy)-1,3-dioxolan-4-yl]oxy}acetic acid.

[18] Ng C,DeWitt JC.Addressing urgent questions for PFAS in the 21st century.Environ Sci Technol2021;55:12755-65 PMCID:PMC8590733

[19] Podder A,Reinhart D,Goel R.Per and poly-fluoroalkyl substances (PFAS) as a contaminant of emerging concern in surface water: a transboundary review of their occurrences and toxicity effects.J Hazard Mater2021;419:126361

[20] Bernardini I,Valsecchi S.The new PFAS C6O4 and its effects on marine invertebrates: first evidence of transcriptional and microbiota changes in the Manila clam Ruditapes philippinarum.Environ Int2021;152:106484

[21] Fabrello J,Masiero L.New compounds, old problems. The case of C6O4 - a substitute of PFOA - and its effects to the clam Ruditapes philippinarum.J Hazard Mater2021;420:126689

[22] Fabrello J,Ciscato M.First evidence of in vitro effects of C6O4 - a substitute of PFOA-on haemocytes of the clam Ruditapes philippinarum.Toxics2021;9:191 PMCID:PMC8402315

[23] Lopez-Antia A,Lasters R.Perfluoroalkyl acids (PFAAs) concentrations and oxidative status in two generations of great tits inhabiting a contamination hotspot.Environ Sci Technol2019;53:1617-26

[24] Lopez-Antia A,Meyer J,Bervoets L.High levels of PFOS in eggs of three bird species in the neighbourhood of a fluoro-chemical plant.Ecotoxicol Environ Saf2017;139:165-71

[25] Blévin P,Tartu S.Perfluorinated substances and telomeres in an Arctic seabird: cross-sectional and longitudinal approaches.Environ Pollut2017;230:360-7

[26] Custer CM,Delaney R,Schultz S.Perfluoroalkyl contaminant exposure and effects in tree swallows nesting at clarks marsh, Oscoda, Michigan, USA.Arch Environ Contam Toxicol2019;77:1-13

[27] Valsecchi S,Mazzoni M.Occurrence and sources of perfluoroalkyl acids in Italian river basins.Chemosphere2015;129:126-34

[28] Hoff PT,Van de Vijver K.Perfluorooctane sulfonic acid and organohalogen pollutants in liver of three freshwater fish species in Flanders (Belgium): relationships with biochemical and organismal effects.Environ Pollut2005;137:324-33

[29] Lopez-Antia A,Müller W,Eens M.Understanding PFAAs exposure in a generalist seabird species breeding in the vicinity of a fluorochemical plant: Influence of maternal transfer and diet.Environ Pollut2021;271:116355

[30] Rusconi M,Stefani F.Evaluating the impact of a fluoropolymer plant on a river macrobenthic community by a combined chemical, ecological and genetic approach.Sci Total Environ2015;538:654-63

[31] Eberhardt LL.Quantitative ecology and impact assessment.J Environ Manag1976;4:27-70

[32] Green RH.Sampling design and statistical methods for environmental biologists. New York: John Wiley & Sons; 1979.

[33] Hoff PT,Van de Vijver K.Biochemical effect evaluation of perfluorooctane sulfonic acid-contaminated wood mice (Apodemus sylvaticus).Environ Health Perspect2004;112:681-6 PMCID:PMC1241962

[34] D’Hollander W,Hagenaars A,Bervoets L.Characterisation of perfluorooctane sulfonate (PFOS) in a terrestrial ecosystem near a fluorochemical plant in Flanders, Belgium.Environ Sci Pollut Res Int2014;21:11856-66

[35] Greaves AK,Sonne C,Born EW.Tissue-specific concentrations and patterns of perfluoroalkyl carboxylates and sulfonates in East Greenland polar bears.Environ Sci Technol2012;46:11575-83

[36] Hoff PT,Dauwe T.Evaluation of biochemical effects related to perfluorooctane sulfonic acid exposure in organohalogen-contaminated great tit (Parus major) and blue tit (Parus caeruleus) nestlings.Chemosphere2005;61:1558-69

[37] Dauwe T,De Coen W.PFOS levels in the blood and liver of a small insectivorous songbird near a fluorochemical plant.Environ Int2007;33:357-61

[38] Groffen T,D’Hollander W,Eens M.Perfluoroalkylated acids in the eggs of great tits (Parus major) near a fluorochemical plant in Flanders, Belgium.Environ Pollut2017;228:140-8

[39] Custer CM,Dummer PM.Legacy and contaminants of emerging concern in tree swallows along an agricultural to industrial gradient: Maumee River, Ohio.Environ Toxicol Chem2020;39:1936-52

[40] Groffen T,Lopez-Antia A,Bervoets L.Limited reproductive impairment in a passerine bird species exposed along a perfluoroalkyl acid (PFAA) pollution gradient.Sci Total Environ2019;652:718-28

[41] Davis KL,Larsen BS,Hartten AS.Transport of ammonium perfluorooctanoate in environmental media near a fluoropolymer manufacturing facility.Chemosphere2007;67:2011-9

[42] Cui Q,Zhang H.Occurrence and tissue distribution of novel perfluoroether carboxylic and sulfonic acids and legacy per/polyfluoroalkyl substances in black-spotted frog (pelophylax nigromaculatus).Environ Sci Technol2018;52:982-90

[43] Lin H,Yang H.Per- and polyfluoroalkyl substances (PFASs) impair lipid metabolism in rana nigromaculata: a field investigation and laboratory study.Environ Sci Technol2022;56:13222-32

[44] Groffen T,Bervoets L.Do concentrations of perfluoroalkylated acids (PFAAs) in isopods reflect concentrations in soil and songbirds?.Sci Total Environ2019;657:111-23

[45] Zhu H.Distribution and partitioning of perfluoroalkyl carboxylic acids in surface soil, plants, and earthworms at a contaminated site.Sci Total Environ2019;647:954-61

[46] Buffagni A,Furse MT.A simple procedure to harmonize class boundaries of assessment systems at the pan-European scale.Environ Sci Policy2007;10:709-24

[47] Rusconi M,Polesello S.Evolutionary toxicology as a tool to assess the ecotoxicological risk in freshwater ecosystems.Water2018;10:490