Skip to main content
Top
Published in: Behavioral and Brain Functions 1/2011

Open Access 01-12-2011 | Research

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

Authors: Marte Haave, Annette Bernhard, Finn K Jellestad, Einar Heegaard, Trond Brattelid, Anne-Katrine Lundebye

Published in: Behavioral and Brain Functions | Issue 1/2011

Login to get access

Abstract

Background

Polychlorinated biphenyls (PCBs) are widespread in the environment, human food and breast milk. Seafood is known to contain nutrients beneficial for the normal development and function of the brain, but also contaminants such as PCBs which are neurotoxic. Exposure to non-coplanar PCBs during brain development can disrupt spontaneous behaviour in mice and lead to hyperactive behaviour. Humans are chronically exposed to the highest relative levels of organochlorines in early childhood during brain development, though usually at doses which do not give clinical symptoms of toxicity. This study aimed to elucidate the developmental and behavioural effects of 2,2',4,4',5,5' hexachlorobiphenyl (PCB153) in mice, mimicking human exposure during gestation and lactation.

Methods

Environmentally relevant doses of PCB153 were added to the experimental diets. Feed concentrations were approximately 0.5, 6.5, and 1500 μg PCB153/kg feed, representing a realistic and a worst case scenario of frequent consumption of contaminated fish. The study also investigated the effects of maternal nutrition, i.e. a standard rodent diet versus a high inclusion of salmon. Mice pups were examined for physical- and reflex development, sensorimotor function and spontaneous behaviour from five days after birth until weaning. A selection of pups were followed until 16 weeks of age and tested for open field behaviour and the acoustic startle response (ASR) with prepulse inhibition (PPI). Blood thyroid hormones and liver enzymes, blood lipids and PCB153 content in fat were examined at 16 weeks. Statistical analyses modelled the three way interactions of diet, PCB exposure and litter size on behaviour, using generalized linear models (GLM) and linear mixed effect models (LME). The litter was used as a random variable. Non-parametric tests were used for pair wise comparisons of biochemical analyses.

Results

Litter size consistently influenced pup development and behaviour. Few lasting PCB153 related changes were observed, but results indicated effects on synchronization of physical development. Perinatal PCB153 exposure appeared to reduce habituation and cause aggression in males, though not statistically significant.

Conclusions

Litter size and maternal diet influenced physical development and function more than PCB153 in perinatally exposed mouse pups and supports the developmental importance of maternal care and the social environment.
Appendix
Available only for authorised users
Literature
1.
go back to reference 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.PubMedCentralCrossRefPubMed 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.PubMedCentralCrossRefPubMed
2.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
3.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
4.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
5.
go back to reference 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.PubMedCentralCrossRefPubMed 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.PubMedCentralCrossRefPubMed
6.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
7.
go back to reference Fox WM: Reflex-ontogeny and behavioural development of the mouse. Anim Behav. 1965, 13: 234-241. 10.1016/0003-3472(65)90041-2.CrossRefPubMed Fox WM: Reflex-ontogeny and behavioural development of the mouse. Anim Behav. 1965, 13: 234-241. 10.1016/0003-3472(65)90041-2.CrossRefPubMed
8.
go back to reference Davison A, Dobbing J: Applied neurochemistry. 1968, Oxford: Blackwell Scientific Davison A, Dobbing J: Applied neurochemistry. 1968, Oxford: Blackwell Scientific
9.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
10.
go back to reference Eriksson P: Developmental neurotoxicology in the neonate--effects of pesticides and polychlorinated organic substances. Arch Toxicol Suppl. 1996, 18: 81-88.CrossRefPubMed Eriksson P: Developmental neurotoxicology in the neonate--effects of pesticides and polychlorinated organic substances. Arch Toxicol Suppl. 1996, 18: 81-88.CrossRefPubMed
11.
go back to reference Eriksson P: Developmental neurotoxicity of environmental agents in the neonate. Neurotoxicology. 1997, 18: 719-726.PubMed Eriksson P: Developmental neurotoxicity of environmental agents in the neonate. Neurotoxicology. 1997, 18: 719-726.PubMed
12.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
13.
go back to reference Eriksson P, Fredriksson A: Developmental neurotoxicity of four ortho-substituted polychlorinated biphenyls in the neonatal mouse. Environ Toxicol Pharmacol. 1996, 1: 155-165. 10.1016/1382-6689(96)00015-4.CrossRefPubMed Eriksson P, Fredriksson A: Developmental neurotoxicity of four ortho-substituted polychlorinated biphenyls in the neonatal mouse. Environ Toxicol Pharmacol. 1996, 1: 155-165. 10.1016/1382-6689(96)00015-4.CrossRefPubMed
14.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
15.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
16.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
17.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
18.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
19.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
20.
go back to reference Wolff MS, Teitelbaum SL, Lioy PJ, Santella RM, Wang RY, Jones RL, Caldwell KL, Sjodin A, Turner WE, Li W: 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.PubMedCentralCrossRefPubMed Wolff MS, Teitelbaum SL, Lioy PJ, Santella RM, Wang RY, Jones RL, Caldwell KL, Sjodin A, Turner WE, Li W: 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.PubMedCentralCrossRefPubMed
21.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
23.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
24.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
26.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
27.
go back to reference 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.PubMedCentralCrossRefPubMed 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.PubMedCentralCrossRefPubMed
28.
go back to reference 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.CrossRef 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.CrossRef
29.
go back to reference 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.PubMedCentralCrossRefPubMed 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.PubMedCentralCrossRefPubMed
30.
go back to reference 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.PubMed 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.PubMed
31.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
32.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
33.
go back to reference Costa LG: Contaminants in fish: risk-benefit considerations. Arh Hig Rada Toksikol. 2007, 58: 367-374.CrossRefPubMed Costa LG: Contaminants in fish: risk-benefit considerations. Arh Hig Rada Toksikol. 2007, 58: 367-374.CrossRefPubMed
37.
go back to reference Boucher O, Bastien CH, Saint-Amour D, Dewailly É, 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.CrossRefPubMed Boucher O, Bastien CH, Saint-Amour D, Dewailly É, 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.CrossRefPubMed
38.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
39.
go back to reference 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.PubMedCentralCrossRefPubMed 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.PubMedCentralCrossRefPubMed
40.
go back to reference Umegaki K, Ikegami S: Feeding fish oil to rats accelerates the metabolism of hexachlorobenzene. J Nutr Sci Vitaminol (Tokyo). 1998, 44: 301-311.CrossRef Umegaki K, Ikegami S: Feeding fish oil to rats accelerates the metabolism of hexachlorobenzene. J Nutr Sci Vitaminol (Tokyo). 1998, 44: 301-311.CrossRef
41.
go back to reference 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.PubMed 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.PubMed
42.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
43.
go back to reference 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. 10.1016/j.etap.2009.03.007.CrossRefPubMed 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. 10.1016/j.etap.2009.03.007.CrossRefPubMed
44.
go back to reference Torstensen BE, Espe M, Sanden M, Stubhaug I, Waagbø R, Hemre GI, Fontanillas R, Nordgarden U, Hevrøy EM, Olsvik P: 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. 10.1016/j.aquaculture.2008.08.025.CrossRef Torstensen BE, Espe M, Sanden M, Stubhaug I, Waagbø R, Hemre GI, Fontanillas R, Nordgarden U, Hevrøy EM, Olsvik P: 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. 10.1016/j.aquaculture.2008.08.025.CrossRef
45.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
46.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
47.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
49.
go back to reference Staskal DF, Diliberto JJ, Birnbaum LS: Disposition of BDE 47 in developing mice. Toxicol Sci. 2006, 90: 309-316. 10.1093/toxsci/kfj098.CrossRefPubMed Staskal DF, Diliberto JJ, Birnbaum LS: Disposition of BDE 47 in developing mice. Toxicol Sci. 2006, 90: 309-316. 10.1093/toxsci/kfj098.CrossRefPubMed
50.
go back to reference Viberg H: Neonatal developmental neurotoxicity of brominated flame retardants, the polybrominated diphenyl ethers (PBDEs). PhD. 2004, Uppsala: Uppsala University Viberg H: Neonatal developmental neurotoxicity of brominated flame retardants, the polybrominated diphenyl ethers (PBDEs). PhD. 2004, Uppsala: Uppsala University
51.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
52.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
53.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
54.
go back to reference Tilson HA: Study design considerations in developmental neurotoxicology. Neurotoxicology and Teratology. 1991, 14: 199-203. 10.1016/0892-0362(92)90017-5.CrossRef Tilson HA: Study design considerations in developmental neurotoxicology. Neurotoxicology and Teratology. 1991, 14: 199-203. 10.1016/0892-0362(92)90017-5.CrossRef
55.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
56.
go back to reference 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 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.
go back to reference 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.PubMedCentralCrossRefPubMed 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.PubMedCentralCrossRefPubMed
58.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
59.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
60.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
61.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
62.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
63.
64.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
65.
go back to reference 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.PubMedCentralCrossRef 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.PubMedCentralCrossRef
66.
go back to reference Paylor R, Crawley JN: Inbred strain differences in prepulse inhibition of the mouse startle response. Psychopharmacology (Berl). 1997, 132: 169-180. 10.1007/s002130050333.CrossRef Paylor R, Crawley JN: Inbred strain differences in prepulse inhibition of the mouse startle response. Psychopharmacology (Berl). 1997, 132: 169-180. 10.1007/s002130050333.CrossRef
67.
go back to reference Piegorsch WW, Haseman JK: Statistical methods for analyzing developmental toxicity data. Teratog Carcinog Mutagen. 1991, 11: 115-133. 10.1002/tcm.1770110302.CrossRefPubMed Piegorsch WW, Haseman JK: Statistical methods for analyzing developmental toxicity data. Teratog Carcinog Mutagen. 1991, 11: 115-133. 10.1002/tcm.1770110302.CrossRefPubMed
68.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
69.
go back to reference Pinheiro JC, Bates DM: Mixed-Effects Models in S and S-PLUS. 2000, New York, NY: Springer-Verlag New York, IncCrossRef Pinheiro JC, Bates DM: Mixed-Effects Models in S and S-PLUS. 2000, New York, NY: Springer-Verlag New York, IncCrossRef
70.
go back to reference Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith GM: Mixed Effects Models and Extensions in Ecology with R. 2009, SpringerCrossRef Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith GM: Mixed Effects Models and Extensions in Ecology with R. 2009, SpringerCrossRef
71.
go back to reference R Development Core Team: R: A language and environment for statistical computing. 2009, R Foundation for Statistical Computing, Vienna, Austria R Development Core Team: R: A language and environment for statistical computing. 2009, R Foundation for Statistical Computing, Vienna, Austria
72.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
73.
go back to reference Masuda Y: Toxic effects of PCB/PCDF to human observed in Yusho and other poisonings. Fukuoka Igaku Zasshi. 2009, 100: 141-155.PubMed Masuda Y: Toxic effects of PCB/PCDF to human observed in Yusho and other poisonings. Fukuoka Igaku Zasshi. 2009, 100: 141-155.PubMed
74.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
75.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
76.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
77.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
78.
go back to reference Ruzzin J, Petersen R, Meugnier E, Madsen L, Lock EJ, Lillefosse H, Ma T, Pesenti S, Sonne SB, Marstrand TT: Persistent organic pollutant exposure leads to insulin resistance syndrome. Environ Health Perspect. 2010, 118: 465-471. 10.1289/ehp.0901321.PubMedCentralCrossRefPubMed Ruzzin J, Petersen R, Meugnier E, Madsen L, Lock EJ, Lillefosse H, Ma T, Pesenti S, Sonne SB, Marstrand TT: Persistent organic pollutant exposure leads to insulin resistance syndrome. Environ Health Perspect. 2010, 118: 465-471. 10.1289/ehp.0901321.PubMedCentralCrossRefPubMed
79.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
Metadata
Title
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
Authors
Marte Haave
Annette Bernhard
Finn K Jellestad
Einar Heegaard
Trond Brattelid
Anne-Katrine Lundebye
Publication date
01-12-2011
Publisher
BioMed Central
Published in
Behavioral and Brain Functions / Issue 1/2011
Electronic ISSN: 1744-9081
DOI
https://doi.org/10.1186/1744-9081-7-3

Other articles of this Issue 1/2011

Behavioral and Brain Functions 1/2011 Go to the issue