Developmental toxicity in white leghorn chickens following in ovo exposure to perfluorooctane sulfonate (PFOS)

Reproductive Toxicology

Volumn 27, Issue 3-4, 2009, Pages 307-318

  Peden Adams, Margie M ^a,b,c   Stuckey, Joyce E ^c   Gaworecki, Kristen M ^d   Berger Ritchie, Jennifer ^e   Bryant, Kathy ^d   Jodice, Patrick G ^f   Scott, Thomas R ^d   Ferrario, Joseph B ^g   Guan, Bing ^g   Vigo, Craig ^g   Boone, J Scott ^g   McGuinn, W David ^h   DeWitt, Jamie C ⁱ   Keil, Deborah E ^e  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^c School of Business and Economics   (United States)

^d CLEMSON UNIVERSITY   (United States)

^e UNIVERSITY OF NEVADA   (United States)

^f U S GEOLOGICAL SURVEY   (United States)

^g U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

^h CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

ⁱ EAST CAROLINA UNIVERSITY   (United States)

Author keywords

ALT; Bird; Brain asymmetry; Cholesterol; Developmental; Embryonic; Immune; In ovo; PFOS

Indexed keywords

IMMUNOGLOBULIN M; IMMUNOGLOBULIN Y; LYSOZYME; PERFLUOROOCTANESULFONIC ACID;

ANIMAL TISSUE; ARTICLE; BODY HEIGHT; BRAIN ASYMMETRY; BRAIN DEVELOPMENT; BRAIN MALFORMATION; CHICKEN; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; EMBRYO; ENZYME ACTIVITY; HATCHING; IMMUNOPATHOLOGY; LIVER WEIGHT; NONHUMAN; SPLEEN SIZE;

ABNORMALITIES, DRUG-INDUCED; ALKANESULFONIC ACIDS; ANIMALS; CHICK EMBRYO; CHICKENS; CROWN-RUMP LENGTH; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; ENVIRONMENTAL POLLUTANTS; FEMALE; FLUOROCARBONS; LIVER; ORGAN SIZE; OVUM; SPLEEN; WING;

AVES; CARTHAMUS TINCTORIUS; GALLUS GALLUS; SPONDIAS PURPUREA;

EID: 64949141120     PISSN: 08906238     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.reprotox.2008.10.009     Document Type: Article

References (116)

1. Moody C.A., and Field J.A. Perfluorinated surfactants and the environmental implications of their use in fire-fighting foams. Environ Sci Technol 34 (2000) 3864-3870
2. Giesy J.P., and Kannan K. Perfluorochemical surfactants in the environment. Environ Sci Technol 36 (2002) 146A-152A
3. Giesy J.P., and Kannan K. Global distribution of perfluorooctane sulfonate in wildlife. Environ Sci Technol 35 (2001) 1339-1342
4. Apelberg B.J., Goldman L.R., Calafat A.M., Herbstman J.B., Kuklenyik Z., and Heidler J. Determination of fetal exposure to polyfluoroalkyl compounds in Baltimore, Maryland. Environ Sci Technol 41 (2007) 3891-3897
5. Calafet A.M., Kuklenyik Z., Reidy J.A., Caudill S.P., Tulley J.S., and Needham L.L. Serum concentrations of 11 polyfluoroalkyl compounds in the U.S. population: data from the National Health and Nutrition Examination Survey (NHANES) 1999-2000. Environ Sci Technol 41 (2007) 2237-2242
6. Calafat A.M., Wong L.-Y., Kuklenyik Z., Reidy J.A., and Needham L. 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 (2007) 1596-1602
7. Olsen G.W., Burris J.M., Burlew M.M., and Mandel J.H. Epidemiologic assessment of worker serum perfluorooctanesulfonate (PFOS) and perfluorooctanoate (PFOA) concentrations and medical surveillance examinations. Occup Environ Med 45 (2003) 260-270
8. Olsen G.W., Church T.R., Miller J.P., Burris J.M., Hansen K.J., Lundberg J.K., et al. Perfluorooctanesulfonate and other fluorochemicals in the serum of American Red Cross adult blood donors. Environ Health Perspect 111 (2003) 1892-1901
9. Olsen G.W., Church T.R., Hansen K.J., Burris J.M., and Butenhoff J.L. Quantitative evaluation of perfluorooctanesulfonate (PFOS) and other fluorochemicals in the serum of children. J Children's Health 2 (2004) 53-76
10. Kannan K., Koistinen J., Beckmen K., Evans T., Gorzelany J.F., Hansen K.J., et al. Accumulation of perfluorooctane sulfonate in marine mammals. Environ Sci Technol 35 8 (2001) 1593-1598
11. Kannan K., Franson J.C., Bowerman W.W., Hansen K.J., Jones P.D., and Giesy J.P. Perfluorooctane sulfonate in fish-eating water birds including bald eagles and albatrosses. Environ Sci Technol 35 15 (2001) 3065-3070
12. Kannan K., Corsolini S., Falandysz J., Fillman G., Kummar K.S., Loganathan B.G., et al. Perfluorooctanesulfonate in human blood from several countries. Environ Sci Technol 38 (2004) 4489-4495
13. Kannan K., Tao L., Sinclair E., Pastva S.D., Jude D.J., and Giesy J.P. Perfluorinated compounds in aquatic organisms at various trophic levels in a Great Lakes food chain. Arch Environ Contam Toxicol 48 4 (2005) 559-566
14. Houde M., Wells R.S., Fair P.A., Bossart E.D., Hohn A.A., Rowles T.K., et al. Polyfluoroalkyl compounds in free-ranging bottlenose dolphins (Tursiops truncatus) from the Gulf of Mexico and the Atlantic Ocean. Environ Sci Technol 3 (2005) 6591-6598
15. Houde M., Bujas T.A.D., Small J., Wells R.S., Fair P.A., Bossart E.D., et al. Muir DCG Biomagnification of perfluoroalkyl compounds in the bottlenose dolphin food web. Environ Sci Technol 40 (2006) 4138-4144
16. Keller J.M., Kannan K., Taniyasu S., Yamashita N., Day R.D., Arendt M.D., et al. Perfluorinated compounds in the plasma of loggerhead and Kemp's ridley sea turtles from the southeastern coast of the United States. Environ Sci Technol 39 (2005) 9101-9108
17. Bustnes J.O., Borgå K., Erikstad K.E., Lorentsen S.H., and Herzke D. Perfluorinated, brominated, and chlorinated contaminants in a population of lesser black-backed gulls (Larus fuscus). Environ Toxicol Chem 27 6 (2008) 1383-1392
18. Molina E.D., Balander R., Fitzgerald S.D., Giesy J.P., Kannan K., Mitchell R., et al. 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 (2006) 227-232
19. Verreault J., Houde M., Gabrielsen G.W., Berger U., Haukås M., Letcher R.J., et al. Perfluorinated alkyl substances in plasma, liver, brain, and eggs of glaucous gulls (Larus hyperboreus) from the Norwegian arctic. Environ Sci Technol 39 19 (2005) 7439-7445
20. Verreault J., Berger U., and Gabrielsen G.W. Trends of perfluorinated alkyl substances in herring gull eggs from two coastal colonies in northern Norway: 1983-2003. Environ Sci Technol 41 19 (2007) 6671-6677
21. Kennedy G.L. Dermal toxicity of ammonium perfluorooctanoate. Toxicol Appl Pharmacol 81 (1985) 348-355
22. Kennedy G.L. Increase in mouse liver weight following feeding of ammonium perfluorooctanoate and related fluorochemicals. Toxicol Lett 39 (1987) 295-300
23. Pastoor T.P., Lee K.P., Perri M.A., and Gillies P.J. Biochemical and morphological studies of ammonium perfluorooctanoate-induced hepatomegaly and peroxisome proliferation. Exp Mol Pathol 47 (1987) 98-109
24. Cook J.C., Murray S.M., Frame S.R., and Hurtt M.E. Induction of Leydig cell adenomas by ammonium perfluorooctanoate; a possible endocrine-related mechanism. Toxicol Appl Pharmacol 113 (1992) 209-217
25. Biegel L.B., Hurtt M.E., Frame S.R., O'Connor J.C., and Cook J.C. Mechanisms of extrahepatic tumor induction by peroxisome proliferators in male CD rats. Toxicol Sci 60 (2001) 44-55
26. Shipley J.M., Hurst C.H., Tanaka S.S., DeRoos F.L., Butenhoff J.L., Seacat A.M., et al. Trans-activation of PPAR-alpha and induction of PPAR-alpha target genes by perfluorooctane-based chemicals. Toxicol Sci 80 1 (2004) 151-160
27. Luebker D.L., Hansen K.J., Bass N.M., Butenhoff J.L., and Seacat A.M. Interaction of flurochemicals with rat liver fatty acid-binding protein. Toxicology 176 (2002) 175-185
28. OECD. Hazard assessment of perfuorooctane sulfonate (PFOS) and its salts. ENV/JM/RD(2002)17/Final. ; 2002 [accessed 12.05.04].
29. Seacat A.M., Thomford P.J., Hansent K.J., Olsen G.W., Case M.T., and Butenhoff J.L. Subchronic toxicity studies on perfluorooctanesulfonate potassium salt in cynomolgus monkeys. Toxicol Sci 68 (2002) 249-264
30. Seacat A.M., Thomford P.J., Hansen K.J., Clemen L.A., Eldridge S.R., Elcombe C.R., et al. Sub-chronic dietary toxicity of potassium perfluorooctanesulfonate in rats. Toxicology 183 (2003) 117-131
31. Thibodeaux J.R., Hanson R.G., Rogers J.M., Grey B.E., Barbee B.D., Richards J.H., et al. Exposure to perfluorooctane sulfonate during pregnancy in rat and mouse. I. Maternal and prenatal evaluations. Toxicol Sci 74 (2003) 369-381
32. Fort D., Rodgers R.L., Guiney P.D., and Weeks J.A. Effects of perfluorooctanesulfonate (PFOS) exposure on steroidogensis in juvenile Xenopus (Silurana) tropicalis. Society of environmental toxicology and chemistry-abstract book, 28th annual meeting. November 11-15th, Milwaukee, WI (2007 231)
33. Ankley G.T., Kuehl D.W., Kahl M.D., Jensen K.M., Linnum A., Leine R.L., et al. Reproductive and developmental toxicity and bioconcentration of perfluorooctanesulfonate in a partial life-cycle test with the fathead minnow (Pimephales promelas). Environ Toxicol Chem 24 (1985) 316-2324
34. Fair PA, Driscoll E, Mollenhauer MAM, Bradshaw SG, Yun S, Kannan K, et al. Effects of environmentally relevant levels of perfluorooctane sulfonate (PFOS) on clinical parameters and immunological functions; submitted for publication.
35. Wetzel LT. Rat teratology study, T-3351, final report. Hazelton Laboratories America, Inc. Project number 154-160. December 19, 1983 (8EHQ-0399-374). Available on USEPA Public docket AR-226 (No. 226-0014).
36. Liu R.C., Hurtt M.E., Cook J.C., and Biegel L.B. Effect of the peroxisome proliferator, ammonium perfluorooctanoate (C8) on hepatic aromatase activity in adult male Crl;CD BR (CD) rats. Fundam Appl Toxicol 30 (1996) 220-228
37. Liu R.C., Hahn C., and Hurtt M.E. The direct effect of hepatic peroxisome proliferators on rat Leydig cell function in vitro. Fundam Appl Toxicol 30 (1996) 102-108
38. Yang Q., Xie Y., and Depierre J.W. Effects of peroxisome proliferators on the thymus and spleen of mice. Clin Exp Immunol 122 (2000) 219-266
39. Yang Q., Xie Y., Eriksson A.M., Nelson B.D., and DePierre J.W. Further evidence for the involvement of inhibition of cell proliferation and development in thymic and splenic atrophy induced by the peroxisome proliferator perfluoroctanoic acid in mice. Biochem Pharmacol 62 (2001) 1133-1140
40. Yang Q., Abedi-Valugerdi M., Xie Y., Zhao X., Möller G., Nelson B.D., et al. Potent suppression of the adaptive immune response in mice upon dietary exposure to the potent peroxisome proliferator, perfluorooctanoic acid. Int Immunopharmacol 2 (2002) 389-397
41. Dewitt J.C., Copeland C.B., Strynar M.J., and Luebke R.W. Perfluorooctanoic acid-induced immunomodulation in adult C57BL/6J or C57BL/6N female mice. Environ Health Perspect 116 5 (2008) 644-650
42. Loveless S.E., Hoban D., Sykes G., Frame S.R., and Everds N.E. Evaluation of the immune system in rats and mice administered linear ammonium perfluorooctanoate (APFO). Toxicol Sci 105 1 (2008) 86-96
43. Nelson D.L., Frazier Jr. D.E., Ericson J.E., Tarr M.J., and Mathes L.E. The effects of perfluorodecanoic acid (PDFA) on humoral, cellular, and innate immunity in Fisher 344 rats. Immunopharmacol Immunotoxicol 14 (1992) 925-938
44. Fang X., Zhang L., Feng Y., Zhao Y., and Dai J. Immunotoxic effects of perfluorononanoic acid on BALB/c mice. Toxicol Sci 105 2 (2008) 312-321
45. Peden-Adams M.M., Keller J.M., EuDaly J.G., Berger J., Gilkeson G.S., and Keil D.E. Suppression of humoral immunity in mice following exposure to perfluorooctane sulfonate (PFOS). Toxicol Sci 104 1 (2008) 144-154
46. DeWitt J.C., Shnyra A., Badr M.Z., Loveless S.E., Hoban D., Frame S.R., et al. Immunotoxicity of perfluorooctanoic acid and perfluorooctane sulfonate and the role of peroxisome proliferator-activated receptor alpha. Crit Rev Toxicol 39 1 (2009) 76-94
47. Kannan K., Perrotta E., and Thomas N.J. Association between perfluorinated compounds and pathological conditions in southern sea otters. Environ Sci Technol 40 16 (2006) 4943-4948
48. Case M.T., York R.G., and Christian M.S. Rat and rabbit oral developmental toxicology studies with two perfluorinated compounds. Int J Toxicol 20 (2001) 101-109
49. Fuentes S., Colomina M.T., Vicens P., Franco-Pons N., and Domingo J.L. 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 (2007) 589-598
50. Grasty R.C., Wolf D.C., Grey B.E., Lau C.S., and Rogers J.M. Prenatal window of susceptibility to perfluorooctane sulfonate-induced neonatal mortality in the Sprague-Dawley rat. Birth Defects Res B: Dev Reprod Toxicol 68 (2003) 465-471
51. Grasty R.C., Bjork J.A., Wallace K.B., Wolf D.C., Lau C.S., and Rogers J.M. Effects of prenatal perfluorooctane sulfonate (PFOS) exposure on lung maturation in the perinatal rat. Birth Defects Res B: Dev Reprod Toxicol 74 5 (2005) 405-416
52. Lau C., Thibodeaux J.R., Hanson R.G., Rogers J.M., Grey B.E., Stanton M.E., et al. Exposure to perfluorooctane sulfonate during pregnancy in rat and mouse. II. Postnatal evaluation. Toxicol Sci 74 2 (2003) 382-392
53. Lau C., Butenhoff J.L., and Rogers J.M. The developmental toxicity of perfluoroalkyl acids and their derivatives. Toxicol Appl Pharmacol 198 2 (2004) 231-241
54. Keil D.E., Mehlmann T., Butterworth L., and Peden-Adams M.M. Embryonic exposure to PFOS suppresses immunological function in F1 mice. Toxicol Sci 103 1 (2008) 77-85
55. Newsted J.L., Jones P.D., Coady K., and Giesy J.P. Avian toxicity reference values for perfluorooctane sulfonate. Environ Sci Technol 39 23 (2005) 9357-9362
56. Hoff P.T., Van de Vijver K., Dauwe T., Covaci A., Maervoet J., Eens M., et al. 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 (2005) 1558-1569
57. Cwinn M.A., Jones S.P., and Kennedy S.W. Exposure to perfluorooctane sulfonate or fenofibrate causes PPAR-alpha dependent transcriptional responses in chicken embryo hepatocytes. Comp Biochem Physiol C: Toxicol Pharmacol 148 2 (2008) 165-171
58. Yeung L.W., Guruge K.S., Yamanaka N., Miyazaki S., and Lam P.K. Differential expression of chicken hepatic genes responsive to PFOA and PFOS. Toxicology 237 1-3 (2007) 111-125
59. Peden-Adams M., Alonso K., Godard C., Skipper S., Mashburn W., Hoover J., et al. Effects of environmentally relevant concentrations of 2,3,7,8-TCDD on domestic chicken immune function and CYP450 activity: F1 generation and egg injection studies. Chemosphere 37 9-12 (1998) 1923-1939
60. Peden-Adams M.M., EuDaly J.G., Heesemann L.M., Smythe J., Miller J., Gilkeson G.S., et al. Developmental immunotoxicity of trichloroethylene (TCE): studies in B6C3F1 mice. J Environ Sci Health A: Tox Hazard Subst Environ Eng 41 3 (2006) 249-271
61. Peden-Adams M.M., EuDaly J.G., Lee A.M., Miller J., Keil D.E., and Gilkeson G.S. Developmental effects of trichloroethylene (TCE) on immunity: studies in MRL (+/+) mice. J Environ Sci Health A: Tox Hazard Subst Environ Eng A 43 12 (2008) 1402-1409
62. Dietert R.R., and Holsapple M.P. Methodologies for developmental immunotoxicity (DIT) testing. Methods 41 1 (2007) 123-131
63. Holsapple M.P., Paustenbach D.J., Charnley G., West L.J., Luster M.I., Dietert R.R., et al. Symposium summary: children's health risk-what's so special about the developing immune system?. Toxicol Appl Pharmacol 199 1 (2004) 61-70
64. Holsapple M.P., Burns-Naas L.A., Hastings K.L., Ladics G.S., Lavin A.L., Makris S.L., et al. A proposed testing framework for developmental immunotoxicology (DIT). Toxicol Sci 83 1 (2005) 18-24
65. Weeks B.A., Anderson D.P., DuFour A.P., Fairbrother A., Goven A.J., Lahvis G.P., et al. Immunological biomarkers to assess environmental stress. In: Huggett R.J., Kimerle R.A., Mehrle Jr. P.M., and Bergman H.L. (Eds). Biomarkers: biochemical, physiological, and histological markers of anthropogenic stress (1992), Lewis Publishers, Boca Raton (FL) 211-234
66. Fairbrother A., Smits J., and Grasman K. Avian immunotoxicology. J Toxicol Environ Health B: Crit Rev 7 2 (2004) 105-137
67. Henshel D.S., DeWitt J., and Troutman A. Avian egg injections. In: Maines M.D., Costa L.G., Hodgson E., Reed D.J., and Sipes I.G. (Eds). Current protocols in toxicology vol. S14 (2002) 13.4.1-13.4.19
68. Scott T.R., and Savage M.L. Immune cell proliferation in the harderian gland: an avian model. Microsc Res Technol 34 (1996) 149-155
69. Grasman K.A., Fox G.A., Scanlon P.F., and Ludwig J.P. Organochlorine-associated immunosuppression in prefledgling caspian terns and herring gulls from the Great Lakes: an ecoepidemiological study. Environ Health Perspect 104 S4 (1996) 829-842
70. In: Hudson L., and Hay F.C. (Eds). Practical immunology (1989), Blackwell Scientific, Oxford 252-254
71. Henshel D.S. Developmental neurotoxic effects of dioxin and dioxin-like compounds on domestic and wild avian species. Environ Toxicol Chem 17 (1998) 88-98
72. Henshel D.S., Martin J.W., and DeWitt J.C. Brain asymmetry as a potential biomarker for developmental TCDD intoxication: a dose-response study. Environ Health Perspect 105 7 (1997) 718-725
73. Harr K.E. Clinical chemistry of companion avian species: a review. Vet Clin Path 31 3 (2002) 140-151
74. Doneley B. Biochemistries: What they do and don't do. In: Proceeding of the small animal veterinary association. 32nd Annual congress, Sydney, Australia, August 19-23, 2007. [accessed June 2008].
75. Smith K.G., and Hunt J.L. On the use of spleen mass as a measure of avian immune system strength. Oecologia 138 (2004) 28-31
76. Ali N.M.H., and Behnke J.M. Observations on the gross changes in the secondary lymphoid organs of mice infected with Nematospiroides dubius. J Helminthol 59 (1985) 167-174
77. John J.L. The avian spleen: a neglected organ. Q Rev Biol 69 (1994) 327-351
78. John J.L. Parasites and the avian spleen: helminths. Biol J Linnean Soc 54 (1995) 87-106
79. Molyneux D.H., Cooper J.E., and Smith W.J. Studies on the pathology of an avian trypanosome (T. bouffardi) infection in experimentally infected canaries. Parasitology 87 (1983) 49-54
80. Vincent A.L., and Ash L.R. Splenomegaly in birds (Meriones unguiculatus) infected with Brugia malayi (Nematoda: Filarioidea) and related species. Am J Trop Med Hyg 27 (1979) 514-520
81. Watkins R.A., Moshier S.E., O'Dell W.D., and Pinter A.J. Splenomegaly and reticulocytosis caused by Babesia microti infections in natural populations of the montane vole, Microtus montanus. J Protozool 38 (1991) 573-576
82. Henshel D.S., Martin J.W., Norstrom R., Whitehead P., Steeves J.D., and Cheng K.M. Morphometric abnormalities in brains of great blue heron hatchlings exposed in the wild to PCDDs. Environ Health Perspect 103 S4 (1995) 61-66
83. Henshel DS, Martin JW, Best D, Cheng KM, Elliott JE, Rosenstein D, et al. Evaluating gross brain asymmetry: A potential biomarker for 2,3,7,8-tetrachlorodibenzo-p-dioxin-related neurotoxicity. In: Bengtson DA, Henshel DS, editors. Environmental toxicology and risk assessment: biomarkers and risk assessment, vol. 5th, ASTM STP 1306 American Society for Testing and Materials, Philadelphia; 1996. p. 230-8.
84. Henshel D.S., Martin J.W., Norstrom R.J., Elliott J., Cheng K.M., and DeWitt J.C. Morphometric brain abnormalities in double-crested cormorant chicks exposed to polychlorinated dibenzo-p-dioxins, dibenzofurans, and biphenyls. J Great Lakes Res 23 1 (1997) 11-26
85. Uhlíkova P., Paclt I., Vaneckova M., Morcinek T., Seidel Z., Krasensky J., et al. Asymmetry of basal ganglia in children with attention deficit hyperactivity disorder. Neuro Endocrinol Lett 28 5 (2007) 604-609
86. Herbert M.R., Ziegler D.A., Deutsch C.K., O'Brien L.M., Kennedy D.N., Filipek P.A., et al. Brain asymmetries in autism and developmental language disorder: a nested whole-brain analysis. Brain 128 1 (2005) 213-226
87. Leonard C.M., Lombardino L.J., Walsh K., Eckert M.A., Mockler J.L., Rowe L.A., et al. Anatomical risk factors that distinguish dyslexia from SLI predict reading skill in normal children. J Commun Disord 35 6 (2002) 501-531
88. Leonard C., Eckert M., Given B., Virginia B., and Eden G. Individual differences in anatomy predict reading and oral language impairments in children. Brain 129 12 (2006) 3329-3342
89. Leonard C.M., Kuldau J.M., Maron L., Ricciuti N., Mahoney B., Bengtson M., et al. Identical neural risk factors predict cognitive deficit in dyslexia and schizophrenia. Neuropsychology 22 2 (2008) 147-158
90. Johansson N., Fredriksson A., and Eriksson P. Neonatal exposure to perfluorooctane sulfonate (PFOS) and perfluorooctanoic acid (PFOA) causes neurobehavioural defects in adult mice. Neurotoxicology 29 1 (2008) 160-169
91. Fuentes S., Vicens P., Colomina M.T., and Domingo J.L. Behavioral effects in adult mice exposed to perfluorooctane sulfonate (PFOS). Toxicology 242 1-3 (2007) 123-129
92. Austin M.E., Kasturi B.S., Barber M., Kannan K., MohanKumar P.S., and MohanKumar S.M. Neuroendocrine effects of perfluorooctane sulfonate in rats. Environ Health Perspect 111 12 (2003) 1485-1489
93. Burton J.E., Dorociak I.R., Schwedler T.E., and Rice C.D. Circulating lysozyme and hepatic CYP1A activities during a chronic dietary exposure to tributyltin (TBT) and 3,3′,4,4′,5-pentachlorobiphenyl (PCB-126) mixtures in channel catfish, Ictalurus punctatus. J Toxicol Environ Health A 65 (2002) 589-602
94. Greenfield J., and Bigland C.H. Detection of lysozyme in developing avian embryos. Poult Sci 50 6 (1971) 1748-1753
95. Board R.G., and Fuller R. Non-specific antimicrobial defenses of the avian egg, embryo, and neonate. Biol Rev 49 (1977) 15-49
96. Guiney P, Talent L, Melson D, EuDaly J, Kannan K, Peden-Adams MM. Immunological alterations in western fence lizards following oral exposure to PFOS. The Toxicologist, (Supplement to Toxicological Sciences); 2007, 96(S-1).
97. Peden-Adams MM, Kannan K, EuDaly J, Hessemann L, Kucklick JR, Arendt MD, et al. Perfluorinated hydrocarbons measured in sea turtle blood correlate to modulations in plasma chemistry values and immune function measurements. In: Society of environmental toxicology and chemistry (SETAC), 25th annual meeting-abstract book; 2004.
98. Peden-Adams MM, Romano T, Rice CD, EuDaly J, Hessemann L, Muir D, et al. Immune function and clinical blood parameters correlate with perfluorinated hydrocarbon concentrations in bottlenose dolphins. In: Society of environmental toxicology and chemistry (SETAC), 25th annual meeting-abstract book; 2004.
99. Osserman E.F., and Lawlor D.P. Serum and urinary lysozyme (muramidase) in monocytic and monomyelocytic leukemia. J Exp Med 124 (1966) 921-952
100. Brierre J., Barthelemy J., Bachard G., and Fiet J. Interet de la Determination de L'Activite Muramidasique Serique et Urinaire dans les Syndromes Myeloproliferatifs Chroniques, Subaigus et les Myeloblastoses Partielles. II. Application a Divers Cas Pathologiques. Clin Chim Acta 50 (1974) 265
101. Falchuk K.R., Perrotto J.L., and Isselbacher K.J. Serum lysozyme in Crohn's disease and ulcerative colitis. NEJM 292 8 (1975) 395-397
102. Hughes W.T., Koblin B.A., and Rosenstein B.J. Lysozyme activity in cystic fibrosis. Pediatr Res 16 10 (1982) 874-876
103. Torsteinsdóttir I., Håkansson L., Hällgren R., Gudbjörnsson B., Arvidson N.-G., and Venge P. Serum lysozyme: a potential marker of monocyte/macrophage activity in rheumatoid arthritis. Rheumatology 38 (1999) 1249-1254
104. Fernandez-de-Mera I.G., Vicente J., Hofle U., Rodriguez O., Gaspar-Lopez E., and Gortazar C. The effects of sex and age on phytohaemagglutinin skin-testing of deer. NZ Vet J 56 2 (2008) 71-73
105. Warren DC. Distinguishing sex of chicks at hatching. Bulletin 307, agricultural experiment station, kansas state college of agriculture and applied science. ; 1942 [accessed June 2008].
106. Furuya M., Sasaki F., Hassanin A.M.A., Kuwahara S., and Tsukamoto Y. Effects of bisphenol-A on the growth of comb and testes of male chicken. Can J Vet Res 67 (2003) 68-71
107. Burlington H., and Lindeman V.F. Effect of DDT on testes and secondary sex characteristics of white leghorn cockerels. Proceedings of the society for experimental biology and medicine, vol. 74 (1950) 48-51
108. Blomqvist A., Berg C., Holm L., Brandt I., Ridderstrale Y., and Brunstrom B. Defective reproductive organ morphology and function in domestic rooster embryonically exposed to o,p-DDT or ethynylestradiol. Biol Reprod 74 (2006) 481-486
109. Mayer J.A., Chuong C.-M., and Widelitz M.R. Rooster feathering, androgenic alopecia, and hormone-dependent tumor growth: what is in common?. Differentiation 72 (2004) 474-488
110. Jensen A.A., and Leffers H. Emerging endocrine disrupters: perfluoroalkylated substances. Int J Androl 31 2 (2008) 161-169
111. Peden-Adams M.M., EuDaly J.G., Dabra S., EuDaly A., Heesemann L., Smythe J., et al. Suppression of humoral immunity following exposure to the perfluorinated insecticide sulfluramid. J Toxicol Environ Health Part A 70 (2007) 1130-1141
112. Liu C., Du Y., and Zhou B. Evaluation of estrogenic activities and mechanism of action of perfluorinated chemicals determined by vitellogenin induction in primary cultured tilapia hepatocytes. Aquat Toxicol 85 4 (2007) 267-277
113. Dauwe T., Van de Vijver K., De Coen W., and Eens M. PFOS levels in the blood and liver of a small insectivorous songbird near a fluorochemical plant. Environ Int 33 3 (2007) 357-361
114. Beach S.A., Newsted J.L., Coady K., and Giesy J.P. Ecotoxicological evaluation of perfluorooctanesulfonate (PFOS). Rev Environ Contam Toxicol 186 (2006) 133-174
115. Olivero-Verbel J., Tao L., Johnson-Restrepo B., Guette-Fernández J., Baldiris-Avila R., O'byrne-Hoyos I., et al. Perfluorooctanesulfonate and related fluorochemicals in biological samples from the north coast of Colombia. Environ Pollut 142 2 (2006) 367-372
116. DeWitt J.C., Meyer E.B., and Henshel D.S. Environmental toxicity studies using chickens as surrogates for wildlife: effects of vehicle volume. Arch Environ Contam Toxicol. 48 2 (2005) 260-269