Abnormal neurological responses in young adult offspring caused by excess omega-3 fatty acid (fish oil) consumption by the mother during pregnancy and lactation

Neurotoxicology and Teratology

Volumn 31, Issue 1, 2009, Pages 26-33

  Church, M W ^a   Jen, K L C ^b   Jackson, D A ^a   Adams, B R ^a   Hotra, J W ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WAYNE STATE UNIVERSITY   (United States)

Author keywords

Auditory brainstem response (ABR); Barker hypothesis; Docosahexanoic acid (DHA); Eicosapentanoic acid (EPA); Fetal programming; Fish oil; Hearing loss; Hyperacusis; Lactation; Omega 3 fatty acids ( 3 FA); Omega 6 fatty acids ( 6 FA); Over nutrition; Postnatal; Pregnancy; Prenatal

Indexed keywords

FISH OIL; OMEGA 3 FATTY ACID; SAFFLOWER OIL;

AMPLITUDE MODULATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN DEVELOPMENT; CONTROLLED STUDY; EVOKED BRAIN STEM AUDITORY RESPONSE; FEMALE; GROWTH RETARDATION; HEARING ACUITY; HEARING LOSS; LACTATION; LOUDNESS RECRUITMENT; MALE; NERVE POTENTIAL; NEUROTRANSMISSION; NONHUMAN; NUTRITIONAL DEFICIENCY; OUTCOME ASSESSMENT; OVERNUTRITION; PERCEPTIVE THRESHOLD; PERINATAL PERIOD; PREGNANCY; PRIORITY JOURNAL; RAT; STIMULUS RESPONSE;

AGING; ANALYSIS OF VARIANCE; ANIMALS; DIET; ELECTRODES; FATTY ACIDS, OMEGA-3; FEMALE; HEARING; LACTATION; MALE; PREGNANCY; PREGNANCY OUTCOME; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, WISTAR; SENSORY THRESHOLDS; SYNAPTIC TRANSMISSION;

CARTHAMUS TINCTORIUS; GLYCINE MAX; PIPS; RATTUS; RATTUS NORVEGICUS;

EID: 57249095825     PISSN: 08920362     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ntt.2008.09.001     Document Type: Article

References (76)

1. Akabas S.R., and Deckelbaum R.J. Summary of a workshop on n - 3 fatty acids: current status of recommendations and future directions. Am. J. Clin. Nutr. 83 (2006) 1536S-1538S
2. Anderson J.W., Johnstone B.M., and Remley D.T. Breast-feeding and cognitive development: a meta-analysis. Am. J. Clin. Nutr. 70 (1999) 525-535
3. Arbuckle L.D., Rioux F.M., Mackinnon M.J., Hrboticky N., and Innis S.M. Response of (n - 3) and (n - 6) fatty acids in piglet brain, liver and plasma to increasing, but low, fish oil supplementation of formula. J. Nutr. 121 (1991) 1536-1547
4. Barker D.J. The developmental origins of chronic adult disease. Acta Paediatr. Suppl. 93 (2004) 26-33
5. Barone Jr. S., Stanton M.E., and Mundy W.R. Neurotoxic effects of neonatal triethyltin (TET) exposure are exacerbated with aging. Neurobiol. Aging 16 (1995) 723-735
6. Bourre J.M., Durand G., Erre J.P., and Aran J.M. Changes in auditory brainstem responses in alpha-linolenic acid deficiency as a function of age in rats. Audiology 38 (1999) 13-18
7. Bourre J.M., Francois M., Youyou A., Dumont O., Piciotti M., Pascal G., and Durand G. The effects of dietary alpha-linolenic acid on the composition of nerve membranes, enzymatic activity, amplitude of electrophysiological parameters, resistance to poisons and performance of learning tasks in rats. J. Nutr. 119 (1989) 1880-1892
8. Carlson S.E. Arachidonic acid status of human infants: influence of gestational age at birth and diets with very long chain n - 3 and n - 6 fatty acids. J. Nutr. 126 (1996) 1092S-10928S
9. Carlson S.E. Docosahexaenoic acid and arachidonic acid in infant development. Semin. Neonatol. 6 (2001) 437-449
10. Carlson S.E., Cooke R.J., Rhodes P.G., Peeples J.M., and Werkman S.H. Effect of vegetable and marine oils in preterm infant formulas on blood arachidonic and docosahexaenoic acids. J. Pediatr. 120 (1992) S159-S167
11. Carlson S.E., Cooke R.J., Rhodes P.G., Peeples J.M., Werkman S.H., and Tolley E.A. Long-term feeding of formulas high in linolenic acid and marine oil to very low birth weight infants: phospholipid fatty acids. Pediatric. Res. 30 (1991) 404-412
12. Carlson S.E., Cooke R.J., Werkman S.H., and Tolley E.A. First year growth of preterm infants fed standard compared to marine oil n - 3 supplemented formula. Lipids 27 (1992) 901-907
13. Carlson S.E., Werkman S.H., Peeples J.M., Cooke R.J., and Tolley E.A. Arachidonic acid status correlates with first year growth in preterm infants. Proc. Natl. Acad. Sci. U S A 90 (1993) 1073-1077
14. Cho S.H., and Choi Y.S. Lipid peroxidation and antioxidant status is affected by different vitamin E levels when feeding fish oil. Lipids 29 (1994) 47-52
15. Church M.W., Abel E.L., Kaltenbach J.A., and Overbeck G.W. Effects of prenatal alcohol exposure and aging on auditory function in the rat: preliminary results. Alcohol., Clin. Exp. Res. 20 (1996) 172-179
16. Church M.W., Blakley B.W., Burgio D.L., and Gupta A.K. WR-2721 (Amifostine) ameliorates cisplatin-induced hearing loss but causes neurotoxicity in hamsters: dose-dependent effects. J. Assoc. Res. Otolaryngol. 5 (2004) 227-237
17. Church M.W., and Gritzke R. Effects of ketamine anesthesia on the rat brain-stem auditory evoked potential as a function of dose and stimulus intensity. Electroencephalogr. Clin. Neurophysiol. 67 (1987) 570-583
18. Church M.W., Jen K.-L.C., Stafferton T., Hotra J.W., and Adams B.R. Reduced auditory acuity in rat pups from excess and deficient omega-3 fatty acid consumption by the mother. Neurotoxicol. Teratol. 29 (2007) 203-210
19. Church M.W., Jen K.L., Dowhan L.M., Adams B.R., and Hotra J.W. Excess and deficient omega-3 fatty acid during pregnancy and lactation cause impaired neural transmission in rat pups. Neurotoxicol. Teratol. 30 (2008) 107-117
20. Church M.W., Williams H.L., and Holloway J.A. Postnatal development of the brainstem auditory evoked potential and far-field cochlear microphonic in non-sedated rat pups. Brain Res. 316 (1984) 23-31
21. Davis H. Brain stem and other responses in electric response audiometry. Ann. Otol. Rhinol. Laryngol. 85 (1976) 3-14
22. Fleming T.P., Kwong W.Y., Porter R., Ursell E., Fesenko I., Wilkins A., Miller D.J., Watkins A.J., and Eckert J.J. The embryo and its future. Biol. Reprod. 71 (2004) 1046-1054
23. Fritsche K.L., and Johnston P.V. Rapid autoxidation of fish oil in diets without added antioxidants. J. Nutr. 118 (1988) 425-426
24. Gonzalez M.J., Gray J.I., Schemmel R.A., Dugan Jr. L., and Welsch C.W. Lipid peroxidation products are elevated in fish oil diets even in the presence of added antioxidants. J. Nutr. 122 (1992) 2190-2195
25. Grandjean P., Bjerve K.S., Weihe P., and Steuerwald U. Birthweight in a fishing community: significance of essential fatty acids and marine food contaminants. Int. J. Epidemiol. 30 (2001) 1272-1278
26. Grandjean P., and Weihe P. Neurobehavioral effects of intrauterine mercury exposure: potential sources of bias. Environ. Res. 61 (1993) 176-183
27. Hadders-Algra M., Bouwstra H., van Goor S.A., Dijck-Brouwer D.A., and Muskiet F.A. Prenatal and early postnatal fatty acid status and neurodevelopmental outcome. J. Perinat. Med. 35 Suppl 1 (2007) S28-S34
28. Hagve T.A., Christensen E., Gronn M., and Christophersen B.O. Regulation of the metabolism of polyunsaturated fatty acids. Scand. J. Clin. Lab. Invest. 191 (1988) 33-46
29. Hardy S.C., and Kleinman R.E. Fat and cholesterol in the diet of infants and young children: implications for growth, development, and long-term health. J. Pediatr. 125 (1994) S69-S77
30. Haubner L.Y., Stockard J.E., Saste M.D., Benford V.J., Phelps C.P., Chen L.T., Barness L., Wiener D., and Carver J.D. Maternal dietary docosahexanoic acid content affects the rat pup auditory system. Brain Res. Bull. 58 (2002) 1-5
31. Henry K.R. Auditory brainstem volume-conducted responses: origins in the laboratory mouse. J. Am. Audit. Soc. 4 (1979) 173-178
32. Herrera E., Lopez-Soldado I., Limones M., Amusquivar E., and Ramos M.P. Lipid metabolism during the perinatal phase, and its implications on postnatal development. Int. J. Vitam. Nutr. Res. 76 (2006) 216-224
33. Innis S.M. The role of dietary n - 6 and n - 3 fatty acids in the developing brain. Dev. Neurosci. 22 (2000) 474-480
34. Janicke B., and Coper H. The effects of prenatal exposure to hypoxia on the behavior of rats during their life span. Pharmacol. Biochem. Behav. 48 (1994) 863-873
35. K.-L.C. Jen, M.W. Church, C. Wang, M. Moghaddam, L. DoWhan, F. Laja, J. Sherman, Perinatal omega-3 fatty acid imbalance affects the fatty acid composition in rat offspring, submitted for publication
36. Jensen C.L. Effects of n - 3 fatty acids during pregnancy and lactation. Am. J. Clin. Nutr. 83 (2006) 1452S-1457S
37. Jensen C.L., Prager T.C., Fraley J.K., Chen H., Anderson R.E., and Heird W.C. Effect of dietary linoleic/alpha-linolenic acid ratio on growth and visual function of term infants. J. Pediatr. 131 (1997) 200-209
38. Koutz C.A., Wiegand R.D., Rapp L.M., and Anderson R.E. Effect of dietary fat on the response of the rat retina to chronic and acute light stress. Exp. Eye Res. 60 (1995) 307-316
39. Kwong W.Y., Wild A.E., Roberts P., Willis A.C., and Fleming T.P. Maternal undernutrition during the preimplantation period of rat development causes blastocyst abnormalities and programming of postnatal hypertension. Development 127 (2000) 4195-4202
40. Lauritzen L., Jorgensen M.H., Olsen S.F., Straarup E.M., and Michaelsen K.F. Maternal fish oil supplementation in lactation: effect on developmental outcome in breast-fed infants. Reprod. Nutr. Dev. 45 (2005) 535-547
41. Lucia Bergmann R., Bergmann K.E., Haschke-Becher E., Richter R., Dudenhausen J.W., Barclay D., and Haschke F. Does maternal docosahexaenoic acid supplementation during pregnancy and lactation lower BMI in late infancy?. J. Perinat. Med. 35 (2007) 295-300
42. Makrides M., Duley L., and Olsen S.F. Marine oil, and other prostaglandin precursor, supplementation for pregnancy uncomplicated by pre-eclampsia or intrauterine growth restriction. Cochrane Database Syst. Rev. 3 (2006) CD003402
43. Markel E., Felszeghy K., Luiten P.G., and Nyakas C. Beneficial effect of chronic nimodipine treatment on behavioral dysfunctions of aged rats exposed to perinatal ethanol treatment. Arch. Gerontol. Geriatr. 21 (1995) 75-88
44. Martin J.C. Irreversible changes in mature and aging animals following intrauterine drug exposure. Neurobehav. Toxicol. Teratol. 8 (1986) 335-343
45. Naeye R.L., Blanc W., and Paul C. Effects of maternal nutrition on the human fetus. Pediatrics 52 (1973) 494-503
46. National Institute of Child Health and Human DevelopmentOmega-3 fatty acid: a randomized trial of omega-3 fatty acid supplementation to prevent preterm birth in pregnancies at high risk Clin. Trials NCT00135902. Available on http://clinicaltrials.gov/ct2/show/NCT00135902?term=nichd+(Clinical+Trials) & rank=12
47. Nyakas C., Buwalda B., and Luiten P.G. Hypoxia and brain development. Prog. Neurobiol. 49 (1996) 1-51
48. Oken E., Kleinman K.P., Olsen S.F., Rich-Edwards J.W., and Gillman M.W. Associations of seafood and elongated n - 3 fatty acid intake with fetal growth and length of gestation: results from a US pregnancy cohort. Am. J. Epidemiol. 160 (2004) 774-783
49. Olsen S.F., Hansen H.S., Sorensen T.I., Jensen B., Secher N.J., Sommer S., and Knudsen L.B. Hypothesis: dietary (N - 3)-fatty acids prolong gestation in human beings. Prog. Clin. Biol. Res. 242 (1987) 51-56
50. Olsen S.F., and Secher N.J. A possible preventive effect of low-dose fish oil on early delivery and pre-eclampsia: indications from a 50-year-old controlled trial. Br. J. Nutr. 64 (1990) 599-609
51. Olsen S.F., Sorensen J.D., Secher N.J., Hedegaard M., Henriksen T.B., Hansen H.S., and Grant A. Randomised controlled trial of effect of fish-oil supplementation on pregnancy duration. Lancet 339 (1992) 1003-1007
52. Pembrey M.E., Bygren L.O., Kaati G., Edvinsson S., Northstone K., Sjostrom M., and Golding J. Sex-specific, male-line transgenerational responses in humans. Eur. J. Hum. Genet. 14 (2006) 159-166
53. Phillips D.P., and Carr M.M. Disturbances of loudness perception. J. Am. Acad. Audiol 9 (1998) 371-379 quiz 399
54. Plagemann A., Heidrich I., Gotz F., Rohde W., and Dorner G. Obesity and enhanced diabetes and cardiovascular risk in adult rats due to early postnatal overfeeding. Exp. Clin. Endocrinol. 99 (1992) 154-158
55. Reeves P.G., Nielsen F.H., and Fahey Jr. G.C. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J. Nutr. 123 (1993) 1939-1951
56. Roegge C.S., Widholm J.J., Engeseth N.J., Wang X., Brosch K.O., Seegal R.F., and Schantz S.L. Delayed spatial alternation impairments in adult rats following dietary n - 6 deficiency during development. Neurotoxicol. Teratol. 27 (2005) 485-495
57. Rossi G.T., and Britt R.H. Effects of hypothermia on the cat brain-stem auditory evoked response. Electroencephalogr. Clin. Neurophysiol. 57 (1984) 143-155
58. Rump P., Mensink R.P., Kester A.D., and Hornstra G. Essential fatty acid composition of plasma phospholipids and birth weight: a study in term neonates. Am. J. Clin. Nutr. 73 (2001) 797-806
59. Saste M.D., Carver J.D., Stockard J.E., Benford V.J., Chen L.T., and Phelps C.P. Maternal diet fatty acid composition affects neurodevelopment in rat pups. J. Nutr. 128 (1998) 740-743
60. Sattar N., Berry C., and Greer I.A. Essential fatty acids in relation to pregnancy complications and fetal development. Br. J. Obstet. Gynaecol. 105 (1998) 1248-1255
61. Schallert T. Sensorimotor impairment and recovery of function in brain-damaged rats: reappearance of symptoms during old age. Behav. Neurosci. 97 (1983) 159-164
62. Scott D.T., Janowsky J.S., Carroll R.E., Taylor J.A., Auestad N., and Montalto M.B. Formula supplementation with long-chain polyunsaturated fatty acids: are there developmental benefits?. Pediatrics 102 (1998) E59
63. Sendowski I., Braillon-Cros A., and Delaunay C. CAP amplitude after impulse noise exposure in guinea pigs. Eur. Arch. Otorhinolaryngol. 261 (2004) 77-81
64. Simmer K., and Patole S. Longchain polyunsaturated fatty acid supplementation in preterm infants. Cochrane Database Syst. Rev. (2004) CD000375
65. Smuts C.M., Huang M., Mundy D., Plasse T., Major S., and Carlson S.E. A randomized trial of docosahexaenoic acid supplementation during the third trimester of pregnancy. Obstet. Gynecol. 101 (2003) 469-479
66. Starr A., Sininger Y., Nguyen T., Michalewski H.J., Oba S., and Abdala C. Cochlear receptor (microphonic and summating potentials, otoacoustic emissions) and auditory pathway (auditory brain stem potentials) activity in auditory neuropathy. Ear Hear. 22 (2001) 91-99
67. Stockard J.E., Saste M.D., Benford V.J., Barness L., Auestad N., and Carver J.D. Effect of docosahexaenoic acid content of maternal diet on auditory brainstem conduction times in rat pups. Dev. Neurosci. 22 (2000) 494-499
68. Thorsdottir I., Birgisdottir B.E., Halldorsdottir S., and Geirsson R.T. Association of fish and fish liver oil intake in pregnancy with infant size at birth among women of normal weight before pregnancy in a fishing community. Am. J. Epidemiol. 160 (2004) 460-465
69. Wainwright P.E. Dietary essential fatty acids and brain function: a developmental perspective on mechanisms. Proc. Nutr. Soc. 61 (2002) 61-69
70. Wainwright P.E., Jalali E., Mutsaers L.M., Bell R., and Cvitkovic S. An imbalance of dietary essential fatty acids retards behavioral development in mice. Physiol. Behav. 66 (1999) 833-839
71. Wainwright P.E., Xing H.C., Mutsaers L., McCutcheon D., and Kyle D. Arachidonic acid offsets the effects on mouse brain and behavior of a diet with a low (n - 6):(n - 3) ratio and very high levels of docosahexaenoic acid. J. Nutr. 127 (1997) 184-193
72. Wakefield S.L., Lane M., Schulz S.J., Hebart M.L., Thompson J.G., and Mitchell M. Maternal supply of omega-3 polyunsaturated fatty acids alter mechanisms involved in oocyte and early embryo development in the mouse. Am. J. Physiol. Endocrinol. Metab. 294 (2008) E425-E434
73. Wallace R.B., Daniels C.E., and Altman J. Behavioral effects of neonatal irradiation of the cerebellum. 3. Qualitative observations in aged rats. Dev. Psychobiol. 5 (1972) 35-41
74. Weisinger H.S., Vingrys A.J., and Sinclair A.J. The effect of docosahexaenoic acid on the electroretinogram of the guinea pig. Lipids 31 (1996) 65-70
75. Wu G., Bazer F.W., Cudd T.A., Meininger C.J., and Spencer T.E. Maternal nutrition and fetal development. J. Nutr. 134 (2004) 2169-2172
76. Yang G., Lobarinas E., Zhang L., Turner J., Stolzberg D., Salvi R., and Sun W. Salicylate induced tinnitus: behavioral measures and neural activity in auditory cortex of awake rats. Hear. Res. 226 (2007) 244-253