Potential toxicity of environmentally relevant perfluorooctane sulfonate (PFOS) concentrations to yellow-legged gull Larus michahellis embryos

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• 作者：Marco Parolini ; Graziano Colombo…
• 关键词：Perfluorooctane sulfonate (PFOS) ; Embryotoxicity ; Oxidative and genetic damage ; Yellow ; legged gull
• 刊名：Environmental Science and Pollution Research
• 出版年：2016
• 出版时间：January 2016
• 年：2016
• 卷：23
• 期：1
• 页码：426-437
• 全文大小：780 KB
• 参考文献：Ahmad S, Kalra H, Gupta A, Raut B, Hussain A, Rahman MA (2012) HybridSPE: a novel technique to reduce phospholipid-based matrix effect in LC-ESI-MS bioanalysis. J Pharm Bioallied Sci 4(4):267–275CrossRef
  Apelberg BJ, Goldman LR, Calafat AM, Herbstman JB, Kuklenyik Z, Heidler J (2007) Determinants of fetal exposure to polyfluoroalkyl compounds in Baltimore, Maryland. Environ Sci Technol 41(11):3891–3897CrossRef
  Arukwe A, Mortensen AS (2011) Lipid peroxidation and oxidative stress responses of salmon fed a diet containing perfluorooctane sulfonic-or perfluorooctane carboxylic acids. Comp Biochem Physiol C Comp Pharmacol Toxicol 154(4):288–295CrossRef
  Bertolero A, Vicente J, Meyer J, Lacorte S (2015) Accumulation and maternal transfer of perfluorooctane sulphonic acid in yellow-legged (Larus michahellis) and Audouin’s gull (Larus audouinii) from the Ebro Delta Natural Park. Environ Res 137:2018–2214CrossRef
  Boulanger B, Vargo J, Schnoor G, Hornbuckle K (2004) Detection of perfluorooctane surfactants in Great Lakes water. Environ Sci Technol 38(15):4064–4070CrossRef
  Buck RC, Franklin J, Berger U, Conder JM, Cousins IT, de Voogt P, Jensen AA, Kannan K, Mabury SA, van Leeuwen SPJ (2011) Perfluoroalkyl and polyfluoroalkyl substances in the environment: terminology, classification, and origins. Integr Environ Assess Manag 7(4):513–541CrossRef
  Calafat AM, Wong L-Y, Kuklenyik Z, Reidy JA, Needham L (2007) Polyfluoroalkyl chemicals in the U.S. population: data from the National Health and Nutrition Examination Survey (NHANES) 2003–2004 and comparisons to NHANES 1999–2000. Environ Health Perspect 115:1596–1602CrossRef
  Castiglioni S, Valsecchi S, Polesello S, Rusconi M, Melis M, Palmiotto M, Manenti A, Davoli E, Zuccato E (2015) Sources and fate of perfluorinated compounds in the aqueous environment and in drinking water of a highly urbanized and industrialized area in Italy. J Hazard Mater 282:51–60CrossRef
  Chen T, Zhang L, Yue JQ, Lv ZQ, Xia W, Wan YJ, Li Y-Y, Xu SQ (2012) Prenatal PFOS exposure induces oxidative stress and apoptosis in the lung of rat off-spring. Reprod Toxicol 33(4):538–545CrossRef
  Cramp S (1998) The complete birds of the Western Palearctic on CD-ROM. Oxford University Press, Oxford
  Custer CM, Custer TW, Schoenfuss HL, Poganski BH, Solem L (2012) Exposure and effects of perfluoroalkyl compounds on tree swallows nesting at Lake Johanna in east central Minnesota, USA. Reprod Toxicol 33(4):556–562CrossRef
  Custer CM, Custer TW, Dummer PM, Etterson MA, Thogmartin WE, Wu Q, Kannan K, Trowbridge A, McKann PC (2014) Exposure and effects of perfluoroalkyl substances in Tree Swallows nesting in Minnesota and Wisconsin, USA. Arch Environ Contam Toxicol 66:120–138CrossRef
  De Roode DE, Gustavsson MB, Rantalainen AL, Klomp AV, Koeman JH, Bosveld ATC (2002) Embryotoxic potential of persistent organic pollutants extracted from tissues of guillemots (Uria aalge) from the Baltic Sea and the Atlantic Ocean. Environ Toxicol Chem 21(11):2401–2411CrossRef
  Du Y, Shi X, Liu C, Yu K, Zhou B (2009) Chronic effects of water-borne PFOS exposure on growth, survival and hepatotoxicity in zebrafish: a partial life-cycle test. Chemosphere 74(5):723–729CrossRef
  Eng ML, Williams TD, Elliott JE (2013) Developmental exposure to a brominated flame retardant: an assessment of effects on physiology, growth, and reproduction in a songbird, the zebra finch. Environ Pollut 178:343–349CrossRef
  Erel O (2005) A new automated colorimetric method for measuring total oxidant status. Clin Biochem 38(12):1103–1111CrossRef
  European Commission, Directive 2006/122/EC of the European Parliament and of the Council of 12 December 2006 amending for the 30th time Council Directive 76/769/EEC on the approximation of the laws, regulations and administrative provisions of the Member States relating to restrictions on the marketing and use of certain dangerous substances and preparations (perfluorooctane sulfonates). Official Journal of the European Union, 2006, L372/32
  Fang X, Feng Y, Wang J, Dai J (2010) Perfluorononanoic acid-induced apoptosis in rat spleen involves oxidative stress and the activation of caspase-independent death pathway. Toxicology 267(1):54–59CrossRef
  Fuentes S, Colomina MT, Vicens P, Franco-Pons N, Domingo JL (2007) Concurrent exposure to perfluorooctane sulfonate and restraint stress during pregnancy in mice: effects on postnatal development and behavior of the offspring. Toxicol Sci 98(2):589–598CrossRef
  Gad SE (2005) Dimethyl sulfoxide. In: Wexler P (ed) Encyclopedia of toxicology. Elsevier, Amsterdam
  Gebbink WA, Hebert CE, Letcher RJ (2009) Perfluorinated carboxylates and sulfonates and precursor compounds in herring gull eggs from colonies spanning the Laurentian Great Lakes of North America. Environ Sci Technol 43:7443–7449CrossRef
  Gebbink WA, Letcher RJ, Burgess NM, Champoux L, Elliott JE, Hebert CE et al (2011) Perfluoroalkyl carboxylates and sulfonates and precursors in relation to dietary source tracers in the eggs of four species of gulls (Larids) from breeding sites spanning Atlantic to Pacific Canada. Environ Int 37:1175–82
  Giesy JP, Kannan K (2001) Global distribution of perfluorooctane sulfonate in wildlife. Environ Sci Technol 35(7):1339–1342CrossRef
  Giesy JP, Kannan K (2002) Peer reviewed: perfluorochemical surfactants in the environment. Environ Sci Technol 36(7):146A–152ACrossRef
  Griffiths R, Daan S, Dijkstra C (1996) Sex identification in birds using two CHD genes. Proc R Soc London B 263(1374):1251–1256CrossRef
  Haukås M, Berger U, Hop H, Gulliksen B, Gabrielsen GW (2007) Bioaccumulation of per-and polyfluorinated alkyl substances (PFAS) in selected species from the Barents Sea food web. Environ Pollut 148(1):360–371CrossRef
  Heinz GH, Hoffman DJ, Kondrad SL, Erwin CA (2006) Factors affecting the toxicity of methylmercury injected into eggs. Arch Environ Contam Toxicol 50:264–279CrossRef
  Hoff PT, Van de Vijver K, Dauwe T, Covaci A, Maervoet J, Eens M, Blust R, De Coen W (2005) Evaluation of biochemical effects related to perfluorooctane sulfonic acid exposure in organohalogen-contaminated great tit (Parus major) and blue tit (Parus caeruleus) nestlings. Chemosphere 61(11):1558–1569CrossRef
  Jones PD, Hu W, Coen WD, Newsted JL, Giesy JP (2003) Binding of perfluorinated fatty acids to serum proteins. Environ Toxicol Chem 22(11):2639–2649CrossRef
  Kannan K, Franson JC, Bowerman WW, Hansen KJ, Jones PD, Giesy JP (2001) Perfluorooctane sulfonate in fish-eating water birds including bald eagles and albatrosses. Environ Sci Technol 35(15):3065–3070CrossRef
  Kannan K, Corsolini S, Falandysz J, Oehme G, Focardi S, Giesy JP (2002) Perfluorooctanesulfonate and related fluorinated hydrocarbons in marine mammals, fishes, and birds from coasts of the Baltic and the Mediterranean Seas. Environ Sci Technol 36(15):3210–3216CrossRef
  Kannan K, Corsolini S, Falandysz J, Fillman G, Kummar KS, Loganathan BG, Mohd MA, Olivero J, Van Wouwe ON, Ho Yang GJ, Aldous KM (2004) Perfluorooctanesulfonate and related fluorochemicals in human blood from several countries. Environ Sci Technol 38(17):4489–44995CrossRef
  Kannan K, Tao L, Sinclair E, Pastva SD, Jude DJ, Giesy JP (2005) Perfluorinated compounds in aquatic organisms at various trophic levels in a Great Lakes food chain. Arch Environ Contam Toxicol 48(4):559–566CrossRef
  Keil DE, Mehlmann T, Butterworth L, Peden-Adams MM (2008) Gestational exposure to perfluorooctane sulfonate suppresses immune function in B6C3F1 mice. Toxicol Sci 103(1):77–85CrossRef
  Lacina O, Hradkova P, Pulkrabova J, Hajslova J (2011) Simple, high throughput ultra-high performance liquid chromatography/tandem mass spectrometry trace analysis of perfluorinated alkylated substances in food of animal origin: milk and fish. J Chromatog A 1218(28):4312–4321CrossRef
  Liu C, Yu K, Shi X, Wang J, Lam PK, Wu RS, Zhou B (2007) Induction of oxidative stress and apoptosis by PFOS and PFOA in primary cultured hepatocytes of freshwater tilapia (Oreochromis niloticus). Aquat Toxicol 82(2):135–143CrossRef
  Liu L, Liu W, Song J, Yu H, Jin Y, Oami K, Sato I, Saito N, Tsuda S (2009) A comparative study on oxidative damage and distributions of perfluorooctane sulfonate (PFOS) in mice at different postnatal developmental stages. J Toxicol Sci 34(3):245–254CrossRef
  Lucas A, Morales J, Velando A (2014) Differential effects of specific carotenoids on oxidative damage and immune response of gull chicks. J Exp Biol 217(8):1253–1262CrossRef
  Luebker DJ, Hansen KJ, Bass NM, Butenhoff JL, Seacat AM (2002) Interactions of fluorochemicals with rat liver fatty acid-binding protein. Toxicology 176(3):175–185CrossRef
  Mazzoni M, Rusconi M, Valsecchi S, Martins CPB, Polesello S (2015) An on-line solid phase extraction-liquid chromatography-tandem mass spectrometry method for the determination of perfluoroalkyl acids in drinking and surface waters. J Anal Methods Chem Article ID 942016, 13 pp. doi:10.​1155/​2015/​942016
  Mckernan MA, Rattner BA, Hale RC, Ottinger MA (2009) Toxicity of polybrominated diphenyl ethers (de-71) in chicken (Gallus gallus), mallard (Anas platyrhynchos), and American kestrel (Falco sparverius) embryos and hatchlings. Environ Toxicol Chem 28(5):1007–1017CrossRef
  McKernan MA, Rattner BA, Hatfield JS, Hale RC, Ottinger MA (2010) Absorption and biotransformation of polybrominated diphenyl ethers DE-71 and DE-79 in chicken (Gallus gallus), mallard (Anas platyrhynchos), American kestrel (Falco sparverius) and black-crowned night-heron (Nycticorax nycticorax) eggs. Chemosphere 79(1):100–109CrossRef
  Molina ED, Balander R, Fitzgerald SD, Giesy JP, Kannan K, Mitchell R, Bursian SJ (2006) Effects of air cell injection of perfluorooctane sulfonate before incubation on development of the white leghorn chicken (Gallus domesticus) embryo. Environ Toxicol Chem 25(1):227–232CrossRef
  Moody CA, Field JA (2000) Perfluorinated surfactants and the environmental implications of their use in fire-fighting foams. Environ Sci Technol 34(18):3864–3870CrossRef
  Newsted JL, Beach SA, Gallagher SP, Giesy JP (2006) Pharmacokinetics and acute lethality of perfluorooctanesulfonate (PFOS) to juvenile mallard and northern bobwhite. Arch Environ Contam Toxicol 50(3):411–420CrossRef
  Newsted JL, Coady KK, Beach SA, Butenhoff JL, Gallagher S, Giesy JP (2007) Effects of perfluorooctane sulfonate on mallard and northern bobwhite quail exposed chronically via the diet. Environ Toxicol Pharmacol 23(1):1–9CrossRef
  Nisbet ICT (1978) Dependence of fledging success on egg-size, parental performance and egg composition among common and roseate terns, Sterna hirundo and S. dougallii. Ibis 120(2):207–215CrossRef
  Oakes K, Sibley P, Martin J, MacLean D, Solomon K, Mabury S, Van Der Kraak G (2005) Short-term exposures of fish to perfluorooctane sulfonate: acute effects on fatty acyl-CoA oxidase activity, oxidative stress, and circulating sex steroids. Environ Toxicol Chem 24(5):1172–1181CrossRef
  O’Brien JM, Carew AC, Chu S, Letcher RJ, Kennedy SW (2009) Perfluorooctane sulfonate (PFOS) toxicity in domestic chicken (Gallus gallus domesticus) embryos in the absence of effects on peroxisome proliferator activated receptor alpha (PPARα)-regulated genes. Comp Biochem Physiol C Comp Pharmacol Toxicol 149(4):524–530CrossRef
  Olive PL (1988) DNA precipitation assay: a rapid and simple method for detecting DNA damage in mammalian cells. Environ Mol Mutagen 11(4):487–495CrossRef
  Olsen GW, Burris JM, Burlew MM, Mandel JH (2003) Epidemiologic assessment of worker serum perfluorooctanesulfonate (PFOS) and perfluorooctanoate (PFOA) concentrations and medical surveillance examinations. J Occup Environ Med 45(3):260–270CrossRef
  Organization for Economic Cooperation and Development (OECD) Environment Directorate (2002) Hazard assessment of perfluorooctane sulfonate (PFOS) and its salts. http://​www.​oecd.​org/​chemicalsafety/​risk-assessment/​2382880.​pdf
  Ottinger MA, Lauoie E, Thompson N, Barton A, Whitehouse K, Barton M, Viglietti-Panzica C (2008) Neuroendocrine and behavioral effects of embryonic exposure to endocrine disrupting chemicals in birds. Brain Res Rev 57(2):376–385CrossRef
  Parolini M, Romano M, Caprioli M, Rubolini D, Saino N (2015) Vitamin E deficiency in last-laid eggs limits growth of yellow-legged gull chicks. Funct Ecol 29(8):1070–1077
  Peden-Adams MM, Stuckey JE, Gaworecki KM, Berger-Ritchie J, Bryant K, Jodice PG, Scott TR, Ferrario JB, Guan B, Vigo C, Boone JS, McGuinn WD, DeWitt JC, Keil DE (2009) Developmental toxicity in white leghorn chickens following in ovo exposure to perfluorooctane sulfonate (PFOS). Reprod Toxicol 27(3):307–318CrossRef
  Prevedouros K, Cousins IT, Buck RC, Korzeniowski SH (2006) Sources, fate and transport of perfluorocarboxylates. Environ Sci Technol 40:32–44CrossRef
  Pusch K (2005) Gull eggs—food of high organic pollutant content? J Environ Monit 7(6):635–639CrossRef
  Romano M, Caprioli M, Ambrosini R, Rubolini D, Fasola M, Saino N (2008) Maternal allocation strategies and differential effects of yolk carotenoids on the phenotype and viability of yellow‐legged gull (Larus michahellis) chicks in relation to sex and laying order. J Evol Biol 21(6):1626–1640CrossRef
  Rubolini D, Romano M, Martinelli R, Saino N (2006) Effects of elevated yolk testosterone levels on survival, growth and immunity of male and female yellow-legged gull chicks. Behav Ecol Sociobiol 59:344–352
  Rubolini D, Romano M, Navara KJ, Karadas F, Ambrosini R, Caprioli M, Saino N (2011) Maternal effects mediated by egg quality in the Yellow-legged Gull Larus michahellis in relation to laying order and embryo sex. Front Zool 8:24
  Rubolini D, Romano M, Boncoraglio G, Ferrari RP, Martinelli R, Galeotti P, Fasola M, Saino N (2005) Effects of elevated egg corticosterone levels on behavior, growth, and immunity of yellow-legged gull (Larus michahellis) chicks. Horm Behav 47:592–605
  Saino N, Martinelli R, Romano M (2008) Ecological and phenological covariates of offspring sex ratio in barn swallows. Evol Ecol 22(5):659–674CrossRef
  Seacat AM, Thomford PJ, Hansen KJ, Olsen GW, Case MT, Butenhoff JL (2002) Subchronic toxicity studies on perfluorooctanesulfonate potassium salt in cynomolgus monkeys. Toxicol Sci 68(1):249–264CrossRef
  Seacat AM, Thomford PJ, Hansen KJ, Clemen LA, Eldridge SR, Elcombe CR, Butenhoff JL (2003) Subchronic dietary toxicity of potassium perfluorooctanesulfonate in rats. Toxicology 183(1):117–131CrossRef
  Shi XJ, Zhou BS (2010) The role of Nrf2 and MAPK pathways in PFOS-induced oxidative stress in zebrafish embryos. Toxicol Sci 115(2):391–400CrossRef
  Shi X, Yeung LW, Lam PK, Wu RS, Zhou B (2009) Protein profiles in zebrafish (Danio rerio) embryos exposed to PFOS. Toxicol Sci 111
  Thibodeaux JR, Hanson RG, Rogers JM, Grey BE, Barbee BD, Richards JH, Butenhoff JL, Stevenson LA, Lau C (2003) Exposure to perfluorooctane sulfonate during pregnancy in rat and mouse. I: maternal and prenatal evaluations. Toxicol Sci 74(2):369–381CrossRef
  United Nations Environmental Programme (UNEP) (2009) Report of the Conference of the Parties of the Stockholm Convention on persistent organic pollutants on the work of its fourth meeting. UNEP, Geneva. http://​chm.​pops.​int/​Portals/​0/​Repository/​COP4/​UNEP-POPS-COP.​4-38.​English.​pdf
  Valsecchi S, Rusconi M, Mazzoni M, Viviano G, Pagnotta R, Zaghi C, Serrini G, Polesello S (2014) Occurrence and sources of perfluoroalkyl acids in Italian river basins. Chemosphere
  Verboven N, Verreault J, Letcher RJ, Gabrielsen GW, Evans NP (2008) Maternally derived testosterone and 17β-estradiol in the eggs of Arctic
  eeding glaucous gulls in relation to persistent organic pollutants. Comp Biochem Physiol C Comp Pharmacol Toxicol 148(2):143–151CrossRef
  Verlecar XN, Jena KB, Chainy GBN (2008) Modulation of antioxidant defences in digestive gland of Perna viridis (L.), on mercury exposures. Chemosphere 71(10):1977–1985CrossRef
  Verreault J, Agudo Villa R, Gabrielsen GW, Skaare JU, Letcher RJ (2006) Maternal transfer of organohalogen contaminants and metabolites to eggs of Arctic
  eeding glaucous gulls. Environ Pollut 144:1053–1060
  Vicente J, Bertolero A, Meyer J, Viana P, Lacorte S (2012) Distribution of perfluorinated compounds in Yellow-legged gull eggs (Larus michahellis) from the Iberian Peninsula. Sci Total Environ 416:468–475CrossRef
  Vicente J, Sanpera C, García-Tarrasón M, Pérez A, Lacorte S (2015) Perfluoroalkyl and polyfluoroalkyl substances in entire clutches of Audouin’s gulls from the Ebro delta. Chemosphere 119:S62–S68CrossRef
  Winter V, Elliott JE, Letcher RJ, Williams TD (2013) Validation of an egg-injection method for embryotoxicity studies in a small, model songbird, the zebra finch (Taeniopygia guttata). Chemosphere 90(1):125–131CrossRef
  
• 作者单位：Marco Parolini (1)
  Graziano Colombo (1)
  Sara Valsecchi (2)
  Michela Mazzoni (2)
  Cristina Daniela Possenti (1)
  Manuela Caprioli (1)
  Isabella Dalle-Donne (1)
  Aldo Milzani (1)
  Nicola Saino (1)
  Diego Rubolini (1)
  
  1. Department of Biosciences, University of Milan, via Celoria 26, I-20133, Milan, Italy
  2. IRSA-CNR–Water Research Institute, National Research Council, Via Mulino 19, I-20861, Brugherio, MB, Italy
  
• 刊物类别：Earth and Environmental Science
• 刊物主题：Environment
  Environment
  Atmospheric Protection, Air Quality Control and Air Pollution
  Waste Water Technology, Water Pollution Control, Water Management and Aquatic Pollution
  Industrial Pollution Prevention
  
• 出版者：Springer Berlin / Heidelberg
• ISSN：1614-7499

文摘

Perfluooctane sulfonate (PFOS) is considered an emerging pollutant because of its wide distribution in both aquatic and terrestrial ecosystems, as well as its potential toxicity to living organisms. Although PFOS environmental levels and the adverse effects on classical model organisms in toxicological studies are well known, including developmental alterations and alteration of oxidative status, its toxicity to free-living species has been seldom investigated. The aim of this study was to assess the potential toxicity of environmental levels of PFOS to yellow-legged gull (Larus michahellis) embryos under field experimental conditions. In a within-clutch experimental design, we injected two PFOS concentrations (100 ng PFOS/g egg weight and 200 ng PFOS/g egg weight) in ovo soon after laying. Eggs were collected when they reached the cracking stage. We investigated the effects of PFOS treatment, laying order and sex on both morphological and biochemical endpoints of embryos. Specifically, we assessed changes in embryo body mass and tarsus length, as well as in liver and brain mass. Moreover, the imbalance of oxidative status was evaluated in both liver and brain from embryos by measuring total antioxidant capacity (TAC) and total oxidant status (TOS), while the levels of protein carbonyl content (PCO) and DNA fragmentation were measured as oxidative and genetic damage endpoints, respectively. The concentrations of PFOS we tested did not significantly alter the morphological endpoints, independently of laying order and sex. Similarly, embryo oxidative status and oxidative and genetic damage were not significantly affected by PFOS in ovo exposure. These findings suggest that current environmental PFOS levels do not affect early development of yellow-legged gull embryos.