Long-term effects of environmentally relevant doses of 2,2',4,4',5,5' hexachlorobiphenyl (PCB153) on neurobehavioural development, health and spontaneous behaviour in maternally exposed mice

Behavioral and Brain Functions

Volumn 7, Issue , 2011, Pages

  Haave, Marte ^a,b   Bernhard, Annette ^a,b   Jellestad, Finn K ^b   Heegaard, Einar ^c   Brattelid, Trond ^a   Lundebye, Anne Katrine ^a,b  

^a INSTITUTE OF MARINE RESEARCH   (Norway)

^b UNIVERSITY OF BERGEN   (Norway)

^c NORWEGIAN INSTITUTE OF BIOECONOMY RESEARCH   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

2,2',4,4',5,5' HEXACHLOROBIPHENYL; CASEIN; LIPID; LIVER ENZYME; PCB 153; THYROID HORMONE; UNCLASSIFIED DRUG; 2,4,5,2',4',5'-HEXACHLOROBIPHENYL; POLYCHLORINATED BIPHENYL;

ACOUSTIC REFLEX; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CHEMICAL ANALYSIS; COGNITION; CONTAMINATED FISH; CONTROLLED STUDY; DRUG EFFECT; EXPERIMENTAL STUDY; FEEDING BEHAVIOR; FEMALE; FISH; FOOD INTAKE; GESTATION PERIOD; GROWTH RATE; HABITUATION; LACTATION; LIPID BLOOD LEVEL; LITTER SIZE; MALE; MATERNAL CARE; MATERNAL NUTRITION; MOUSE; NONHUMAN; NONPARAMETRIC TEST; PERINATAL PERIOD; PHYSICAL DEVELOPMENT; PREPULSE INHIBITION; PRIORITY JOURNAL; PROGENY; RANDOMIZATION; RANDOMIZED CONTROLLED TRIAL; RODENT; SALMON; SENSORIMOTOR FUNCTION; STARTLE REFLEX; STATISTICAL MODEL; THYROTROPIN BLOOD LEVEL; WEANING; WEIGHT GAIN; ADIPOSE TISSUE; ANIMAL; BAGG ALBINO MOUSE; BLOOD; CHEMISTRY; DOSE RESPONSE; ENVIRONMENTAL EXPOSURE; ENZYMOLOGY; EXPLORATORY BEHAVIOR; LIVER; PREGNANCY; PRENATAL EXPOSURE; PSYCHOLOGICAL ASPECT;

ADIPOSE TISSUE; ANIMALS; BEHAVIOR, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; EXPLORATORY BEHAVIOR; FEMALE; LIPIDS; LITTER SIZE; LIVER; MALE; MATERNAL EXPOSURE; MICE; MICE, INBRED BALB C; POLYCHLORINATED BIPHENYLS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; STARTLE REACTION; THYROID HORMONES;

EID: 78651298177     PISSN: None     EISSN: 17449081     Source Type: Journal    
DOI: 10.1186/1744-9081-7-3     Document Type: Article

References (79)

1. Guvenius DM, Aronsson A, Ekman-Ordeberg G, Bergman A, Noren K. Human prenatal and postnatal exposure to polybrominated diphenyl ethers, polychlorinated biphenyls, polychlorobiphenylols, and pentachlorophenol. Environ Health Perspect 2003, 111:1235-1241. 10.1289/ehp.5946, 1241580, 12842779.
2. Noren K, Meironyte D. Certain organochlorine and organobromine contaminants in Swedish human milk in perspective of past 20-30 years. Chemosphere 2000, 40:1111-1123. 10.1016/S0045-6535(99)00360-4, 10739053.
3. Polder A, Skaare JU, Skjerve E, Loken KB, Eggesbo M. Levels of chlorinated pesticides and polychlorinated biphenyls in Norwegian breast milk (2002-2006), and factors that may predict the level of contamination. Sci Total Environ 2009, 407:4584-4590. 10.1016/j.scitotenv.2009.04.032, 19457543.
4. Lignell S, Aune M, Darnerud PO, Cnattingius S, Glynn A. Persistent organochlorine and organobromine compounds in mother's milk from Sweden 1996-2006: compound-specific temporal trends. Environ Res 2009, 109:760-767. 10.1016/j.envres.2009.04.011, 19477439.
5. Schecter A, Pavuk M, Papke O, Ryan JJ, Birnbaum L, Rosen R. Polybrominated diphenyl ethers (PBDEs) in U.S. mothers' milk. Environ Health Perspect 2003, 111:1723-1729. 10.1289/ehp.6466, 1241714, 14594622.
6. Meironyte D, Noren K, Bergman A. Analysis of polybrominated diphenyl ethers in Swedish human milk. A time-related trend study, 1972-1997. J Toxicol Environ Health A 1999, 58:329-341. 10.1080/009841099157197, 10580757.
7. Fox WM. Reflex-ontogeny and behavioural development of the mouse. Anim Behav 1965, 13:234-241. 10.1016/0003-3472(65)90041-2, 5835840.
8. Davison A, Dobbing J. Applied neurochemistry. 1968, Oxford: Blackwell Scientific.
9. Eriksson P, Viberg H, Jakobsson E, Orn U, Fredriksson A. A brominated flame retardant, 2,2',4,4',5-pentabromodiphenyl ether: uptake, retention, and induction of neurobehavioral alterations in mice during a critical phase of neonatal brain development. Toxicol Sci 2002, 67:98-103. 10.1093/toxsci/67.1.98, 11961221.
10. Eriksson P. Developmental neurotoxicology in the neonate--effects of pesticides and polychlorinated organic substances. Arch Toxicol Suppl 1996, 18:81-88.
11. Eriksson P. Developmental neurotoxicity of environmental agents in the neonate. Neurotoxicology 1997, 18:719-726.
12. Eriksson P, Ankarberg E, Viberg H, Fredriksson A. The developing cholinergic system as target for environmental toxicants, nicotine and polychlorinated biphenyls (PCBs): implications for neurotoxicological processes in mice. Neurotox Res 2001, 3:37-51. 10.1007/BF03033229, 15111260.
13. Eriksson P, Fredriksson A. Developmental neurotoxicity of four ortho-substituted polychlorinated biphenyls in the neonatal mouse. Environ Toxicol Pharmacol 1996, 1:155-165.
14. Viberg H, Fredriksson A, Jakobsson E, Orn U, Eriksson P. Neurobehavioral derangements in adult mice receiving decabrominated diphenyl ether (PBDE 209) during a defined period of neonatal brain development. Toxicol Sci 2003, 76:112-120. 10.1093/toxsci/kfg210, 12915714.
15. Jacobson JL, Jacobson SW. Intellectual impairment in children exposed to polychlorinated biphenyls in utero. N Engl J Med 1996, 335:783-789. 10.1056/NEJM199609123351104, 8703183.
16. Huisman M, Koopman-Esseboom C, Fidler V, Hadders-Algra M, van der Paauw CG, Tuinstra LG, Weisglas-Kuperus N, Sauer PJ, Touwen BC, Boersma ER. Perinatal exposure to polychlorinated biphenyls and dioxins and its effect on neonatal neurological development. Early Hum Dev 1995, 41:111-127. 10.1016/0378-3782(94)01611-R, 7601016.
17. Eriksson P. Effects of 3,3',4,4'-tetrachlorobiphenyl in the brain of the neonatal mouse. Toxicology 1988, 49:43-48. 10.1016/0300-483X(88)90172-2, 3131929.
18. Donahue DA, Dougherty EJ, Meserve LA. Influence of a combination of two tetrachlorobiphenyl congeners (PCB 47; PCB 77) on thyroid status, choline acetyltransferase (ChAT) activity, and short- and long-term memory in 30-day-old Sprague-Dawley rats. Toxicology 2004, 203:99-107. 10.1016/j.tox.2004.06.011, 15363586.
19. Hallgren S, Darnerud PO. Polybrominated diphenyl ethers (PBDEs), polychlorinated biphenyls (PCBs) and chlorinated paraffins (CPs) in rats-testing interactions and mechanisms for thyroid hormone effects. Toxicology 2002, 177:227-243. 10.1016/S0300-483X(02)00222-6, 12135626.
20. Wolff MS, Teitelbaum SL, Lioy PJ, Santella RM, Wang RY, Jones RL, Caldwell KL, Sjodin A, Turner WE, Li W, et al. Exposures among pregnant women near the World Trade Center site on 11 September 2001. Environ Health Perspect 2005, 113:739-748. 10.1289/ehp.7694, 1257600, 15929898.
21. Brouwer A, Morse DC, Lans MC, Schuur AG, Murk AJ, Klasson-Wehler E, Bergman A, Visser TJ. Interactions of persistent environmental organohalogens with the thyroid hormone system: mechanisms and possible consequences for animal and human health. Toxicol Ind Health 1998, 14:59-84.
22. Non-cancer health effects of polychlorobiphenyls (PCBs) in animals. Comparison of potencies of individual PCB congeners on non-cancer endpoints in animal studies. , http://www.efsa.europa.eu/en/scdocs/doc/284ax2.pdf
23. Tan Y, Chen CH, Lawrence D, Carpenter DO. Ortho-substituted PCBs kill cells by altering membrane structure. Toxicol Sci 2004, 80:54-59. 10.1093/toxsci/kfh119, 15056809.
24. Tan Y, Song R, Lawrence D, Carpenter DO. Ortho-substituted but not coplanar PCBs rapidly kill cerebellar granule cells. Toxicol Sci 2004, 79:147-156. 10.1093/toxsci/kfh108, 15056819.
25. Opinion of the Scientific Panel on contaminants in the food chain on a request from the commission related to the presence of non dioxin-like polychlorinated biphenyls (PCB) in feed and food. , http://www.efsa.europa.eu/en/scdocs/scdoc/284.htm
26. Wood SL, Beyer BK, Cappon GD. Species comparison of postnatal CNS development: functional measures. Birth Defects Res B Dev Reprod Toxicol 2003, 68:391-407. 10.1002/bdrb.10037, 14745989.
27. Suvorov A, Takser L. Facing the challenge of data transfer from animal models to humans: the case of persistent organohalogens. Environ Health 2008, 7:58. 10.1186/1476-069X-7-58, 2596097, 19014546.
28. Braff DL, Geyer MA, Swerdlow NR. Human studies of prepulse inhibition of startle: normal subjects, patient groups, and pharmacological studies. Psychopharmacology (Berl) 2001, 156:234-258. 10.1007/s002130100810, 11549226.
29. Bonham MP, Duffy EM, Robson PJ, Wallace JM, Myers GJ, Davidson PW, Clarkson TW, Shamlaye CF, Strain JJ, Livingstone MB. Contribution of fish to intakes of micronutrients important for fetal development: a dietary survey of pregnant women in the Republic of Seychelles. Public Health Nutr 2009, 12:1312-1320. 10.1017/S136898000800387X, 18986594.
30. Bourre JM. Effects of nutrients (in food) on the structure and function of the nervous system: update on dietary requirements for brain. Part 1: micronutrients. J Nutr Health Aging 2006, 10:377-385.
31. Thomsen C, Knutsen HK, Liane VH, Froshaug M, Kvalem HE, Haugen M, Meltzer HM, Alexander J, Becher G. Consumption of fish from a contaminated lake strongly affects the concentrations of polybrominated diphenyl ethers and hexabromocyclododecane in serum. Mol Nutr Food Res 2008, 52:228-237. 10.1002/mnfr.200700123, 18186101.
32. Darnerud PO, Atuma S, Aune M, Bjerselius R, Glynn A, Grawe KP, Becker W. Dietary intake estimations of organohalogen contaminants (dioxins, PCB, PBDE and chlorinated pesticides, e.g. DDT) based on Swedish market basket data. Food Chem Toxicol 2006, 44:1597-1606. 10.1016/j.fct.2006.03.011, 16730400.
33. Costa LG. Contaminants in fish: risk-benefit considerations. Arh Hig Rada Toksikol 2007, 58:367-374.
34. Opinion of the scientific panel on contaminants in the food chain on a request from the European Parliament related to the safety assessment of wild and farmed fish. , http://www.efsa.europa.eu/cs/BlobServer/Scientific-Opinion/contam-opinion-ej236-swaff-v2-en1.pdf?ssbinary=true
35. Scientific Advisory Commitee on Nutrition Annual Report 2004. , http://www.sacn.gov.uk/reports-position-statements/annual-reports/annual-report-2004.html
36. Joint FAO/WHO expert consultation on the risks and benefits of fish consumption. Executive summary. , http://www.who.int/foodsafety/chem/meetings/RBfish-exec-summary.pdf
37. Boucher O, Bastien CH, Saint-Amour D, Dewailly T, Ayotte P, Jacobson JL, Jacobson SW, Muckle G. Prenatal exposure to methylmercury and PCBs affects distinct stages of information processing: An event-related potential study with Inuit children. NeuroToxicology 2010, 31:373-384. 10.1016/j.neuro.2010.04.005, 20403381.
38. Alsharif NZ, Hassoun EA. Protective effects of vitamin A and vitamin E succinate against 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD)-induced body wasting, hepatomegaly, thymic atrophy, production of reactive oxygen species and DNA damage in C57BL/6J mice. Basic Clin Pharmacol Toxicol 2004, 95:131-138.
39. Peraza MA, Ayala-Fierro F, Barber DS, Casarez E, Rael LT. Effects of micronutrients on metal toxicity. Environ Health Perspect 1998, 106(Suppl 1):203-216. 10.2307/3433921, 1533267, 9539014.
40. Umegaki K, Ikegami S. Feeding fish oil to rats accelerates the metabolism of hexachlorobenzene. J Nutr Sci Vitaminol (Tokyo) 1998, 44:301-311.
41. Morita K, Matsueda T, Iida T. Effect of green tea (matcha) on gastrointestinal tract absorption of polychlorinated biphenyls, polychlorinated dibenzofurans and polychlorinated dibenzo-p-dioxins in rats. Fukuoka Igaku Zasshi 1997, 88:162-168.
42. Passos CJ, Mergler D, Gaspar E, Morais S, Lucotte M, Larribe F, Davidson R, de Grosbois S. Eating tropical fruit reduces mercury exposure from fish consumption in the Brazilian Amazon. Environ Res 2003, 93:123-130. 10.1016/S0013-9351(03)00019-7, 12963396.
43. Folven KI, Glover C, Malde MK, Lundebye AK. Does selenium modify neurobehavioural impacts of developmental methylmercury exposure in mice?. Environ Toxicol Pharmacol 2009, 28:111-119.
44. Torstensen BE, Espe M, Sanden M, Stubhaug I, Waagbø R, Hemre GI, Fontanillas R, Nordgarden U, Hevrøy EM, Olsvik P, et al. Novel production of Atlantic salmon (Salmo salar) protein based on combined replacement of fish meal and fish oil with plant meal and vegetable oil blends. Aquaculture 2008, 285:193-200.
45. Berntssen MH, Julshamn K, Lundebye AK. Chemical contaminants in aquafeeds and Atlantic salmon (Salmo salar) following the use of traditional-versus alternative feed ingredients. Chemosphere 2010, 78:637-646. 10.1016/j.chemosphere.2009.12.021, 20045551.
46. Bjorklund E, Muller A, von Holst C. Comparison of fat retainers in accelerated solvent extraction for the selective extraction of PCBs from fat-containing samples. Anal Chem 2001, 73:4050-4053. 10.1021/ac010178j, 11534735.
47. Muller A, Bjorklund E, von Holst C. On-line clean-up of pressurized liquid extracts for the determination of polychlorinated biphenyls in feedingstuffs and food matrices using gas chromatography-mass spectrometry. J Chromatogr A 2001, 925:197-205. 10.1016/S0021-9673(01)01028-7, 11519806.
48. Seafood data. , http://www.nifes.no/index.php?page-id=137andlang-id=2
49. Staskal DF, Diliberto JJ, Birnbaum LS. Disposition of BDE 47 in developing mice. Toxicol Sci 2006, 90:309-316. 10.1093/toxsci/kfj098, 16407092.
50. Viberg H. Neonatal developmental neurotoxicity of brominated flame retardants, the polybrominated diphenyl ethers (PBDEs). PhD 2004, Uppsala: Uppsala University.
51. Viberg H, Fredriksson A, Eriksson P. Neonatal exposure to polybrominated diphenyl ether (PBDE 153) disrupts spontaneous behaviour, impairs learning and memory, and decreases hippocampal cholinergic receptors in adult mice. Toxicol Appl Pharmacol 2003, 192:95-106. 10.1016/S0041-008X(03)00217-5, 14550744.
52. Viberg H, Fredriksson A, Eriksson P. Investigations of strain and/or gender differences in developmental neurotoxic effects of polybrominated diphenyl ethers in mice. Toxicol Sci 2004, 81:344-353. 10.1093/toxsci/kfh215, 15240897.
53. Viberg H, Johansson N, Fredriksson A, Eriksson J, Marsh G, Eriksson P. Neonatal exposure to higher brominated diphenyl ethers, hepta-, octa-, or nonabromodiphenyl ether, impairs spontaneous behavior and learning and memory functions of adult mice. Toxicol Sci 2006, 92:211-218. 10.1093/toxsci/kfj196, 16611620.
54. Tilson HA. Study design considerations in developmental neurotoxicology. Neurotoxicology and Teratology 1991, 14:199-203.
55. Eriksson P, Darnerud PO. Distribution and retention of some chlorinated hydrocarbons and a phthalate in the mouse brain during the pre-weaning period. Toxicology 1985, 37:189-203. 10.1016/0300-483X(85)90082-4, 3934796.
56. Eriksson P, Fischer C, Fredriksson A. Polybrominated Diphenyl Ethers (PBDEs), a Group of Brominated Flame Retardants, can Interact with PCB in Enhancing Developmental Neurobehavioral Defects. Toxicol Sci 2006,
57. Eriksson P, Jakobsson E, Fredriksson A. Brominated flame retardants: a novel class of developmental neurotoxicants in our environment?. Environ Health Perspect 2001, 109:903-908. 10.1289/ehp.01109903, 1240439, 11673118.
58. Branchi I. The mouse communal nest: investigating the epigenetic influences of the early social environment on brain and behavior development. Neurosci Biobehav Rev 2009, 33:551-559. 10.1016/j.neubiorev.2008.03.011, 18471879.
59. Branchi I, Alleva E, Costa LG. Effects of perinatal exposure to a polybrominated diphenyl ether (PBDE 99) on mouse neurobehavioural development. Neurotoxicology 2002, 23:375-384. 10.1016/S0161-813X(02)00078-5, 12387364.
60. Bignami G, Alleva E, Chiarotti F, Laviola G. Selective changes in mouse behavioral development after prenatal benzodiazepine exposure: a progress report. Prog Neuropsychopharmacol Biol Psychiatry 1992, 16:587-604. 10.1016/0278-5846(92)90017-9, 1496121.
61. Bignami G, Laviola G, Alleva E, Cagiano R, Lacomba C, Cuomo V. Developmental aspects of neurobehavioural toxicity. Toxicol Lett 1992, 64-65(Spec No):231-237. 10.1016/0378-4274(92)90194-O, 1471179.
62. Darnerud PO. Toxic effects of brominated flame retardants in man and in wildlife. Environ Int 2003, 29:841-853. 10.1016/S0160-4120(03)00107-7, 12850100.
63. Bignami G. Economical test methods for developmental neurobehavioral toxicity. Environ Health Perspect 1996, 104(Suppl 2):285-298. 10.2307/3432648, 1469583, 9182035.
64. Glover CN, Zheng D, Jayashankar S, Sales GD, Hogstrand C, Lundebye AK. Methylmercury speciation influences brain gene expression and behavior in gestationally-exposed mice pups. Toxicol Sci 2009, 110:389-400. 10.1093/toxsci/kfp105, 19465457.
65. Swerdlow NR, Weber M, Qu Y, Light GA, Braff DL. Realistic expectations of prepulse inhibition in translational models for schizophrenia research. Psychopharmacology (Berl) 2008, 199:331-388. 10.1007/s00213-008-1072-4, 2771731, 18568339.
66. Paylor R, Crawley JN. Inbred strain differences in prepulse inhibition of the mouse startle response. Psychopharmacology (Berl) 1997, 132:169-180. 10.1007/s002130050333, 9266614.
67. Piegorsch WW, Haseman JK. Statistical methods for analyzing developmental toxicity data. Teratog Carcinog Mutagen 1991, 11:115-133. 10.1002/tcm.1770110302, 1686820.
68. Holson RR, Pearce B. Principles and pitfalls in the analysis of prenatal treatment effects in multiparous species. Neurotoxicol Teratol 1992, 14:221-228. 10.1016/0892-0362(92)90020-B, 1635542.
69. Pinheiro JC, Bates DM. Mixed-Effects Models in S and S-PLUS. 2000, New York, NY: Springer-Verlag New York, Inc.
70. Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith GM. Mixed Effects Models and Extensions in Ecology with R. 2009, Springer.
71. R Development Core Team R: A language and environment for statistical computing. 2009, R Foundation for Statistical Computing, Vienna, Austria, R Development Core Team.
72. Gralewicz S, Wiaderna D, Lutz P, Sitarek K. Neurobehavioural functions in adult progeny of rat mothers exposed to methylmercury or 2,2', 4,4', 5,5'-hexachlorobiphenyl (PCB 153) alone or their combination during gestation and lactation. Int J Occup Med Environ Health 2009, 22:277-291. 10.2478/v10001-009-0020-9, 19819833.
73. Masuda Y. Toxic effects of PCB/PCDF to human observed in Yusho and other poisonings. Fukuoka Igaku Zasshi 2009, 100:141-155.
74. Tilson HA, Jacobson JL, Rogan WJ. Polychlorinated biphenyls and the developing nervous system: cross-species comparisons. Neurotoxicol Teratol 1990, 12:239-248. 10.1016/0892-0362(90)90095-T, 2115098.
75. Bouwknecht JA, Paylor R. Pitfalls in the interpretation of genetic and pharmacological effects on anxiety-like behaviour in rodents. Behavioural Pharmacology 2008, 19:385-402. 10.1097/FBP.0b013e32830c3658, 18690100.
76. Fonio E, Benjamini Y, Sakov A, Golani I. Wild mouse open field behavior is embedded within the multidimensional data space spanned by laboratory inbred strains. Genes Brain Behav 2006, 5:380-388. 10.1111/j.1601-183X.2005.00170.x, 16879632.
77. Darnerud PO, Lignell S, Glynn A, Aune M, Tornkvist A, Stridsberg M. POP levels in breast milk and maternal serum and thyroid hormone levels in mother-child pairs from Uppsala, Sweden. Environ Int 2009, 36:180-187. 10.1016/j.envint.2009.11.001, 19954849.
78. Ruzzin J, Petersen R, Meugnier E, Madsen L, Lock EJ, Lillefosse H, Ma T, Pesenti S, Sonne SB, Marstrand TT, et al. Persistent organic pollutant exposure leads to insulin resistance syndrome. Environ Health Perspect 2010, 118:465-471. 10.1289/ehp.0901321, 2854721, 20064776.
79. Jacobson JL, Jacobson SW. Breast-feeding and gender as moderators of teratogenic effects on cognitive development. Neurotoxicol Teratol 2002, 24:349-358. 10.1016/S0892-0362(02)00197-6, 12009490.