Omega-3 fatty acid and nutrient deficits in adverse neurodevelopment and childhood behaviors

Child and Adolescent Psychiatric Clinics of North America

Volumn 23, Issue 3, 2014, Pages 555-590

  Gow, Rachel V ^a   Hibbeln, Joseph R ^a  

^a NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

Author keywords

Arachidonic acid; Attention deficit hyperactivity disorder; Child neurodevelopment; Conduct disorder; Docosahexaenoic acid; Eicosapentaenoic acid; Learning disorders; Omega 3 fatty acids

Indexed keywords

ALPHA TOCOPHEROL; ARACHIDONIC ACID; CHOLINE; COPPER; DOCOSAHEXAENOIC ACID; FISH OIL; FOLIC ACID; GAMMA LINOLENIC ACID; ICOSANOID; ICOSAPENTAENOIC ACID; IODINE; IRON; LINOLEIC ACID; METHYLPHENIDATE; OMEGA 3 FATTY ACID; OMEGA 6 FATTY ACID; PLACEBO; POLYUNSATURATED FATTY ACID; PRIMROSE OIL; RETINOL; S ADENOSYLMETHIONINE; THYME OIL; VITAMIN B GROUP; ZINC;

ACNE; ACUPUNCTURE; AGGRESSION; ALANINE AMINOTRANSFERASE BLOOD LEVEL; ALLERGIC REACTION; ALPHA TOCOPHEROL DEFICIENCY; ALZHEIMER DISEASE; AMNESIA; ATTENTION DEFICIT DISORDER; BEHAVIOR CHANGE; BLEEDING; BRAIN DEVELOPMENT; BRAIN FUNCTION; BRAIN HEMORRHAGE; CHILD BEHAVIOR; CLINICAL EFFECTIVENESS; CONDUCT DISORDER; DECREASED APPETITE; DEPRESSION; DIARRHEA; DIET; DIET RESTRICTION; DIET SUPPLEMENTATION; DIZZINESS; DRY NOSE; DYSLEXIA; DYSPEPSIA; EMOTION; EVOLUTION; EXERCISE; FAT INTAKE; FATTY ACID BLOOD LEVEL; FATTY ACID METABOLISM; GASTROINTESTINAL HEMORRHAGE; GASTROINTESTINAL PAIN; GASTROINTESTINAL SYMPTOM; HEADACHE; HEART VENTRICLE TACHYCARDIA; HEMOLYTIC ANEMIA; HUMAN; HYPERGLYCEMIA; HYPERICUM; HYPOTENSION; IRON DEFICIENCY; LACTATE DEHYDROGENASE BLOOD LEVEL; LEARNING; LIPOPROTEIN BLOOD LEVEL; LIVER TOXICITY; LOOSE FECES; MAJOR DEPRESSION; MANIA; MEMORY; MENTAL PERFORMANCE; MILD COGNITIVE IMPAIRMENT; MINDFULNESS; MOTOR PERFORMANCE; NAUSEA; NUTRITIONAL DEFICIENCY; NUTRITIONAL REQUIREMENT; PHOTOTHERAPY; PREGNANCY; PRIORITY JOURNAL; PRISONER; PSYCHOSIS; RASH; RESTING STATE NETWORK; REVIEW; SEA FOOD; SUICIDAL BEHAVIOR; UPPER ABDOMINAL PAIN; URTICARIA; ADOLESCENT; ADULT; ANIMAL; BRAIN; CHILD; DRUG EFFECTS; LITERATURE; MALNUTRITION; MENTAL DISORDERS; META ANALYSIS (TOPIC); METABOLISM; PATHOPHYSIOLOGY; RANDOMIZED CONTROLLED TRIAL (TOPIC); TREATMENT OUTCOME; YOUNG ADULT;

ADOLESCENT; ADULT; ANIMALS; BRAIN; CHILD; CHILD BEHAVIOR; DIET; DIETARY SUPPLEMENTS; FATTY ACIDS, OMEGA-3; HUMANS; MALNUTRITION; MENTAL DISORDERS; META-ANALYSIS AS TOPIC; RANDOMIZED CONTROLLED TRIALS AS TOPIC; REVIEW LITERATURE AS TOPIC; TREATMENT OUTCOME; YOUNG ADULT;

EID: 84903381111     PISSN: 10564993     EISSN: 15580490     Source Type: Journal    
DOI: 10.1016/j.chc.2014.02.002     Document Type: Review

References (167)

1. US Department of Agriculture, US Department of Health and Human Services Dietary guidelines for Americans, 2010 2010, U.S. Government Printing Office, Washington, DC. 7th edition.
2. Georgieff M.K. Nutrition and the developing brain: nutrient priorities and measurement. Am J Clin Nutr 2007, 85:614S-620S.
3. Rees G.A., Doyle W., Srivastava A., et al. The nutrient intakes of mothers of low birth weight babies - a comparison of ethnic groups in East London, UK. Matern Child Nutr 2005, 1:91-99.
4. Doyle W., Rees G. Maternal malnutrition in the UK and low birthweight. Nutr Health 2001, 15:213-218.
5. UNICEF Sustainable elimination of iodine deficiency 2008, UNICEF, New York, Available at:. http://www.unicef.org/publications/index_44271.html.
6. The iodine deficiency-way to go yet. Lancet 2008, 372:88. [editorial].
7. Peirano P.D., Algarin C.R., Chamorro R., et al. Sleep and neurofunctions throughout child development: lasting effects of early iron deficiency. JPediatr Gastroenterol Nutr 2009, 48(Suppl 1):S8-S15.
8. Grantham-McGregor S., Ani C. Areview of studies on the effect of iron deficiency on cognitive development in children. JNutr 2001, 131:649S-666S. [discussion: 666S-8S].
9. McCann J.C., Ames B.N. An overview of evidence for a causal relation between iron deficiency during development and deficits in cognitive or behavioral function. Am J Clin Nutr 2007, 85:931-945.
10. Lozoff B. Iron deficiency and child development. Food Nutr Bull 2007, 28:S560-S571.
11. Sachdev H., Gera T., Nestel P. Effect of iron supplementation on mental and motor development in children: systematic review of randomised controlled trials. Public Health Nutr 2005, 8:117-132.
12. Venturi S., Donati F.M., Venturi A., et al. Environmental iodine deficiency: a challenge to the evolution of terrestrial life?. Thyroid 2000, 10:727-729.
13. Coe C.L., Lubach G.R., Bianco L., et al. Ahistory of iron deficiency anemia during infancy alters brain monoamine activity later in juvenile monkeys. Dev Psychobiol 2009, 51:301-309.
14. Lozoff B., Beard J., Connor J., et al. Long-lasting neural and behavioral effects of iron deficiency in infancy. Nutr Rev 2006, 64:S34-S43. [discussion: S72-91].
15. Georgieff M.K. The role of iron in neurodevelopment: fetal iron deficiency and the developing hippocampus. Biochem Soc Trans 2008, 36:1267-1271.
16. Beard J.L., Connor J.R. Iron status and neural functioning. Annu Rev Nutr 2003, 23:41-58.
17. Marszalek J.R., Lodish H.F. Docosahexaenoic acid, fatty acid-interacting proteins, and neuronal function: breastmilk and fish are good for you. Annu Rev Cell Dev Biol 2005, 21:633-657.
18. Karr J.E., Alexander J.E., Winningham R.G. Omega-3 polyunsaturated fatty acids and cognition throughout the lifespan: a review. Nutr Neurosci 2011, 14:216-225.
19. Siegel G., Ermilov E. Omega-3 fatty acids: benefits for cardio-cerebro-vascular diseases. Atherosclerosis 2012, 225:291-295.
20. Innis S.M. Dietary omega 3 fatty acids and the developing brain. Brain Res 2008, 1237:35-43.
21. Haag M. Essential fatty acids and the brain. Can J Psychiatry 2003, 48:195-203.
22. Elmadfa I., Kornsteiner M. Fats and fatty acid requirements for adults. Ann Nutr Metab 2009, 55:56-75.
23. Brenna J.T., Salem N., Sinclair A.J., et al. [alpha]-Linolenic acid supplementation and conversion to n-3 long-chain polyunsaturated fatty acids in humans. Prostaglandins Leukot Essent Fatty Acids 2009, 80:85-91.
24. Crawford M.A., Bazinet R.P., Sinclair A.J. Fat intake and CNS functioning: ageing and disease. Ann Nutr Metab 2009, 55:202-228.
25. Blasbalg T.L., Hibbeln J.R., Ramsden C.E., et al. Changes in consumption of omega-3 and omega-6 fatty acids in the United States during the 20th century. Am J Clin Nutr 2011, 93:950-962.
26. Rett B.S., Whelan J. Increasing dietary linoleic acid does not increase tissue arachidonic acid content in adults consuming Western-type diets: a systematic review. Nutr Metab (Lond) 2011, 8:36.
27. Wood J.D., Enser M., Fisher A.V., et al. Fat deposition, fatty acid composition and meat quality: a review. Meat Sci 2008, 78:343-358.
28. Lauritzen L., Hansen H.S., Jorgensen M.H., et al. The essentiality of long chain n-3 fatty acids in relation to development and function of the brain and retina. Prog Lipid Res 2001, 40:1-94.
29. Brenna J.T., Diau G.Y. The influence of dietary docosahexaenoic acid and arachidonic acid on central nervous system polyunsaturated fatty acid composition. Prostaglandins Leukot Essent Fatty Acids 2007, 77:247-250.
30. Diau G.Y., Hsieh A., Sarkadi-Nagy E., et al. The influence of long chain polyunsaturate supplementation on docosahexaenoic acid and arachidonic acid in baboon neonate central nervous system. BMC Med 2005, 3:11.
31. Mitchell D.C., Gawrisch K., Litman B.J., et al. Why is docosahexaenoic acid essential for nervous system function?. Biochem Soc Trans 1998, 26:365-370.
32. Bourre J.M., Bonneil M., Chaudiere J., et al. Structural and functional importance of dietary polyunsaturated fatty acids in the nervous system. Adv Exp Med Biol 1992, 318:211-229.
33. Jones C.R., Arai T., Rapoport S.I. Evidence for the involvement of docosahexaenoic acid in cholinergic stimulated signal transduction at the synapse. Neurochem Res 1997, 22:663-670.
34. Condray R., Yao J.K., Steinhauer S.R., et al. Semantic memory in schizophrenia: association with cell membrane essential fatty acids. Schizophr Res 2008, 106:13-28.
35. Yehuda S., Rabinovitz S., Mostofsky D.I. Essential fatty acids are mediators of brain biochemistry and cognitive functions. JNeurosci Res 1999, 56:565-570.
36. Tassoni D., Kaur G., Weisinger R.S., et al. The role of eicosanoids in the brain. Asia Pac J Clin Nutr 2008, 17(Suppl 1):220-228.
37. Carlson S.E. Docosahexaenoic acid and arachidonic acid in infant development. Semin Neonatol 2001, 6:437-449.
38. Levant B., Radel J.D., Carlson S.E. Decreased brain docosahexaenoic acid during development alters dopamine-related behaviors in adult rats that are differentially affected by dietary remediation. Behav Brain Res 2004, 152:49-57.
39. McNamara R.K., Carlson S.E. Role of omega-3 fatty acids in brain development and function: potential implications for the pathogenesis and prevention of psychopathology. Prostaglandins Leukot Essent Fatty Acids 2006, 75:329-349.
40. Mostofsky D.I., Yehuda S., Salem N. Fatty acids: physiological and behavioral functions 2001, Humana Press, (NJ).
41. Lands B. Acritique of paradoxes in current advice on dietary lipids. Prog Lipid Res 2008, 47:77-106.
42. Horrobin D.F. Essential fatty acids, prostaglandins, and alcoholism: an overview. Alcohol Clin Exp Res 1987, 11:2-9.
43. Marangoni F., Colombo C., De Angelis L., et al. Cigarette smoke negatively and dose-dependently affects the biosynthetic pathway of the n-3 polyunsaturated fatty acid series in human mammary epithelial cells. Lipids 2004, 39:633-637.
44. Agostoni C., Riva E., Giovannini M., et al. Maternal smoking habits are associated with differences in infants' long-chain polyunsaturated fatty acids in whole blood: a case-control study. Arch Dis Child 2008, 93:414-418.
45. Pawlosky R.J., Salem N. Perspectives on alcohol consumption: liver polyunsaturated fatty acids and essential fatty acid metabolism. Alcohol 2004, 34:27-33.
46. Nakamura M.T., Nara T.Y. Structure, function, and dietary regulation of delta6, delta5, and delta9 desaturases. Annu Rev Nutr 2004, 24:345-376.
47. Brookes K.J., Chen W., Xu X., et al. Association of fatty acid desaturase genes with attention-deficit/hyperactivity disorder. Biol Psychiatry 2006, 60:1053-1061.
48. Simopoulos A.P. The importance of the ratio of omega-6/omega-3 essential fatty acids. Biomed Pharmacother 2002, 56:365-379.
49. Hibbeln J.R., Nieminen L.R., Lands W.E. Increasing homicide rates and linoleic acid consumption among five Western countries, 1961-2000. Lipids 2004, 39:1207-1213.
50. Chalon S. The role of fatty acids in the treatment of ADHD. Neuropharmacology 2009, 57:636-639.
51. Yavin E., Himovichi E., Eilam R. Delayed cell migration in the developing rat brain following maternal omega 3 alpha linolenic acid dietary deficiency. Neuroscience 2009, 162:1011-1022.
52. McNamara R.K., Jandacek R., Rider T., et al. Omega-3 fatty acid deficiency increases constitutive pro-inflammatory cytokine production in rats: relationship with central serotonin turnover. Prostaglandins Leukot Essent Fatty Acids 2010, 83:185-191.
53. Kuipers R.S., Luxwolda M.F., Dijck-Brouwer D.A., et al. Estimated macronutrient and fatty acid intakes from an East African Paleolithic diet. Br J Nutr 2010, 104:1666-1687.
54. Ramsden C.E., Zamora D., Leelarthaepin B., et al. Use of dietary linoleic acid for secondary prevention of coronary heart disease and death: evaluation of recovered data from the Sydney Diet Heart Study and updated meta-analysis. BMJ 2013, 346:e8707.
55. Salem N., Moriguchi T., Greiner R.S., et al. Alterations in brain function after loss of docosahexaenoate due to dietary restriction of n-3 fatty acids. JMol Neurosci 2001, 16:299-307. [discussion: 317-21].
56. Wainwright P.E. Dietary essential fatty acids and brain function: a developmental perspective on mechanisms. Proc Nutr Soc 2002, 61:61-69.
57. Garcia-Calatayud S., Redondo C., Martin E., et al. Brain docosahexaenoic acid status and learning in young rats submitted to dietary long-chain polyunsaturated fatty acid deficiency and supplementation limited to lactation. Pediatr Res 2005, 57:719-723.
58. Al M.D., van Houwelingen A.C., Hornstra G. Long-chain polyunsaturated fatty acids, pregnancy, and pregnancy outcome. Am J Clin Nutr 2000, 71:285S-291S.
59. Alessandri J.M., Guesnet P., Vancassel S., et al. Polyunsaturated fatty acids in the central nervous system: evolution of concepts and nutritional implications throughout life. Reprod Nutr Dev 2004, 44:509-538.
60. Chalon S. Omega-3 fatty acids and monoamine neurotransmission. Prostaglandins Leukot Essent Fatty Acids 2006, 75:259-269.
61. Zimmer L., Delpal S., Guilloteau D., et al. Chronic n-3 polyunsaturated fatty acid deficiency alters dopamine vesicle density in the rat frontal cortex. Neurosci Lett 2000, 284:25-28.
62. Hibbeln J.R., Ferguson T.A., Blasbalg T.L. Omega-3 fatty acid deficiencies in neurodevelopment, aggression and autonomic dysregulation: opportunities for intervention. Int Rev Psychiatry 2006, 18:107-118.
63. Fedorova I., Salem J.N. Omega-3 fatty acids and rodent behavior. Prostaglandins Leukot Essent Fatty Acids 2006, 75:271-289.
64. Mathieu G., Denis S., Lavialle M., et al. Synergistic effects of stress and omega-3 fatty acid deprivation on emotional response and brain lipid composition in adult rats. Prostaglandins Leukot Essent Fatty Acids 2008, 78:391-401.
65. Stein J. The magnocellular theory of developmental dyslexia. Dyslexia 2001, 7:12-36.
66. Antalis C.J., Stevens L.J., Campbell M., et al. Omega-3 fatty acid status in attention-deficit/hyperactivity disorder. Prostaglandins Leukot Essent Fatty Acids 2006, 75:299-308.
67. Ward P.E. Potential diagnostic aids for abnormal fatty acid metabolism in a range of neurodevelopmental disorders. Prostaglandins Leukot Essent Fatty Acids 2000, 63:65-68.
68. Stevens L.J., Zentall S.S., Deck J.L., et al. Essential fatty acid metabolism in boys with attention-deficit hyperactivity disorder. Am J Clin Nutr 1995, 62:761-768.
69. Chen J.R., Hsu S.F., Hsu C.D., et al. Dietary patterns and blood fatty acid composition in children with attention-deficit hyperactivity disorder in Taiwan. JNutr Biochem 2004, 15:467-472.
70. Mitchell E.A., Aman M.G., Turbott S.H., et al. Clinical characteristics and serum essential fatty acid levels in hyperactive children. Clin Pediatr (Phila) 1987, 26:406-411.
71. Mitchell E.A., Lewis S., Cutler D.R. Essential fatty acids and maladjusted behaviour in children. Prostaglandins Leukot Med 1983, 12:281-287.
72. Germano M., Meleleo D., Montorfano G., et al. Plasma, red blood cells phospholipids and clinical evaluation after long chain omega-3 supplementation in children with attention deficit hyperactivity disorder (ADHD). Nutr Neurosci 2007, 10:1-9.
73. Colter A.L., Cutler C., Meckling K. Fatty acid status and behavioural symptoms of Attention Deficit Hyperactivity Disorder in adolescents: a case-control study. Nutr J 2008, 7:8.
74. Richardson A.J., Montgomery P. The Oxford-Durham study: a randomized, controlled trial of dietary supplementation with fatty acids in children with developmental coordination disorder. Pediatrics 2005, 115:1360-1366.
75. Sinn N., Bryan J., Wilson C. Cognitive effects of polyunsaturated fatty acids in children with attention deficit hyperactivity disorder symptoms: a randomised controlled trial. Prostaglandins Leukot Essent Fatty Acids 2008, 78:311-326.
76. Sinn N., Bryan J. Effect of supplementation with polyunsaturated fatty acids and micronutrients on learning and behavior problems associated with child ADHD. JDev Behav Pediatr 2007, 28:82-91.
77. Nemets H., Nemets B., Apter A., et al. Omega-3 treatment of childhood depression: a controlled, double-blind pilot study. Am J Psychiatry 2006, 163:1098-1100.
78. Richardson A.J., Puri B.K. Arandomized double-blind, placebo-controlled study of the effects of supplementation with highly unsaturated fatty acids on ADHD-related symptoms in children with specific learning difficulties. Prog Neuropsychopharmacol Biol Psychiatry 2002, 26:233-239.
79. McNamara R.K., Able J., Jandacek R., et al. Docosahexaenoic acid supplementation increases prefrontal cortex activation during sustained attention in healthy boys: a placebo-controlled, dose-ranging, functional magnetic resonance imaging study. Am J Clin Nutr 2010, 91:1060-1067.
80. Richardson A.J., Burton J.R., Sewell R.P., et al. Docosahexaenoic acid for reading, cognition and behavior in children aged 7-9 years: a randomized, controlled trial (The DOLAB Study). PLoS One 2012, 7:e43909.
81. Kirby A., Woodward A., Jackson S., et al. Adouble-blind, placebo-controlled study investigating the effects of omega-3 supplementation in children aged 8-10 years from a mainstream school population. Res Dev Disabil 2010, 31:718-730.
82. McNamara R.K. The emerging role of omega-3 fatty acids in psychiatry. Prostaglandins Leukot Essent Fatty Acids 2006, 75:223-225.
83. McNamara R.K., Able J., Liu Y., et al. Omega-3 fatty acid deficiency during perinatal development increases serotonin turnover in the prefrontal cortex and decreases midbrain tryptophan hydroxylase-2 expression in adult female rats: dissociation from estrogenic effects. JPsychiatr Res 2009, 43:656-663.
84. Cunnane S.C., Plourde M., Kathy Stewart K., et al. Docosahexaenoic acid and shore-based diets in hominin encephalization: a rebuttal. Am J Human Biol 2007, 19:578-581.
85. Cunnane S.C., Stewart K.M. Human brain evolution: the influence of freshwater and marine food resources 2010, Wiley-Blackwell, Hoboken (NJ).
86. Crawford M.A., Hassam A.G., Williams G. Essential fatty acids and fetal brain growth. Lancet 1976, 1:452-453.
87. Fiennes R.N., Sinclair A.J., Crawford M.A. Essential fatty acid studies in primates linolenic acid requirements of capuchins. JMed Primatol 1973, 2:155-169.
88. Crawford M.A., Leigh Broadhurst C., Guest M., et al. Aquantum theory for the irreplaceable role of docosahexaenoic acid in neural cell signalling throughout evolution. Prostaglandins Leukot Essent Fatty Acids 2013, 88:5-13.
89. Cordain L., Eaton S.B., Sebastian A., et al. Origins and evolution of the Western diet: health implications for the 21st century. Am J Clin Nutr 2005, 81:341-354.
90. Eaton S.B., Eaton S.B., Sinclair A.J., et al. Dietary intake of long-chain polyunsaturated fatty acids during the paleolithic. World Rev Nutr Diet 1998, 83:12-23.
91. Eaton S.B., Eaton S.B., Konner M.J. Paleolithic nutrition revisited: a twelve-year retrospective on its nature and implications. Eur J Clin Nutr 1997, 51:207-216.
92. Crawford M., Crawford S. What we eat today 1972, Stein and Day, New York.
93. Wang Y., Lehane C., Ghebremeskel K., et al. Modern organic and broiler chickens sold for human consumption provide more energy from fat than protein. Public Health Nutr 2010, 13:400-408.
94. Alvheim A.R., Malde M.K., Osei-Hyiaman D., et al. Dietary linoleic acid elevates endogenous 2-AG and anandamide and induces obesity. Obesity (Silver Spring) 2012, 20:1984-1994.
95. Mathers C.D., Loncar D. Projections of global mortality and burden of disease from 2002 to 2030. PLoS Med 2006, 3:e442.
96. Hibbeln J.R., Davis J.M., Steer C., et al. Maternal seafood consumption in pregnancy and neurodevelopmental outcomes in childhood (ALSPAC study): an observational cohort study. Lancet 2007, 369:578-585.
97. US Food and Drug Administration and the Environmental Protection Agency. What you need to know about mercury in fish and shellfish: EPA and FDA advice for women who might become pregnant, women who are pregnant, nursing mothers, and young children. EPA-823-R-04-00 March 2004.
98. Moriguchi T., Greiner R.S., Salem N. Behavioral deficits associated with dietary induction of decreased brain docosahexaenoic acid concentration. JNeurochem 2000, 75:2563-2573.
99. FDA. Draft risk and benefit assessment report and draft summary of published research report of quantitative risk and benefit assessment of commercial fish consumption, focusing on fetal neurodevelopmental effects (measured by verbal development in children) and on coronary heart disease and stroke in the general population, and summary of published research on the beneficial effects of fish consumption and omega-3 fatty acids for certain neurodevelopmental and cardiovascular endpoints. Federal Register-74 FR 3615. Notice of Availability January 21 (Ed.), 2009.
100. Freeman M.P., Mischoulon D., Tedeschini E., et al. Complementary and alternative medicine for major depressive disorder: a meta-analysis of patient characteristics, placebo-response rates, and treatment outcomes relative to standard antidepressants. JClin Psychiatry 2010, 71:682-688.
101. SanGiovanni J.P., Parra-Cabrera S., Colditz G.A., et al. Meta-analysis of dietary essential fatty acids and long-chain polyunsaturated fatty acids as they relate to visual resolution acuity in healthy preterm infants. Pediatrics 2000, 105:1292-1298.
102. Birch E.E., Carlson S.E., Hoffman D.R., et al. The DIAMOND (DHA Intake and Measurement of Neural Development) Study: a double-masked, randomized controlled clinical trial of the maturation of infant visual acuity as a function of the dietary level of docosahexaenoic acid. Am J Clin Nutr 2010, 91:848-859.
103. Forsyth J.S., Willatts P., DiModogno M.K., et al. Do long-chain polyunsaturated fatty acids influence infant cognitive behaviour?. Biochem Soc Trans 1998, 26:252-257.
104. Osendarp S.J., Baghurst K.I., Bryan J., et al. Effect of a 12-mo micronutrient intervention on learning and memory in well-nourished and marginally nourished school-aged children: 2 parallel, randomized, placebo-controlled studies in Australia and Indonesia. Am J Clin Nutr 2007, 86:1082-1093.
105. Stevens L.J., Zentall S.S., Abate M.L., et al. Omega-3 fatty acids in boys with behavior, learning, and health problems. Physiol Behav 1996, 59:915-920.
106. Pawlosky R., Hibbeln J., Lin Y., et al. n-3 fatty acid metabolism in women. Br J Nutr 2003, 90:993-994. [discussion: 994-5].
107. Voigt R.G., Llorente A.M., Jensen C.L., et al. Arandomized, double-blind, placebo-controlled trial of docosahexaenoic acid supplementation in children with attention-deficit/hyperactivity disorder. JPediatr 2001, 139:189-196.
108. Hirayama S., Hamazaki T., Terasawa K. Effect of docosahexaenoic acid-containing food administration on symptoms of attention-deficit/hyperactivity disorder-a placebo-controlled double-blind study. Eur J Clin Nutr 2004, 58(3):467-473.
109. Arnold L.E., Kleykamp D., Votolato N.A., et al. Gamma-linolenic acid for attention-deficit hyperactivity disorder: placebo-controlled comparison to D-amphetamine. Biol Psychiatry 1989, 25:222-228.
110. Belanger S.A., Vanasse M., Spahis S., et al. Omega-3 fatty acid treatment of children with attention-deficit hyperactivity disorder: a randomized, double-blind, placebo-controlled study. Paediatr Child Health 2009, 14:89-98.
111. Raz R., Carasso R.L., Yehuda S. The influence of short-chain essential fatty acids on children with attention-deficit/hyperactivity disorder: a double-blind placebo-controlled study. JChild Adolesc Psychopharmacol 2009, 19:167-177.
112. Sumich A., Matsudaira T., Gow R.V., et al. Resting state electroencephalographic correlates with red cell long-chain fatty acids, memory performance and age in adolescent boys with attention deficit hyperactivity disorder. Neuropharmacology 2009, 57:708-714.
113. Gow R.V., Matsudaira T., Taylor E., et al. Total red blood cell concentrations of omega-3 fatty acids are associated with emotion-elicited neural activity in adolescent boys with attention-deficit hyperactivity disorder. Prostaglandins Leukot Essent Fatty Acids 2009, 80:151-156.
114. Singh S.D., Ellis C.R., Winton A.S., et al. Recognition of facial expressions of emotion by children with attention-deficit hyperactivity disorder. Behav Modif 1998, 22:128-142.
115. Boucher O., Burden M.J., Muckle G., et al. Neurophysiologic and neurobehavioral evidence of beneficial effects of prenatal omega-3 fatty acid intake on memory function at school age. Am J Clin Nutr 2011, 93:1025-1037.
116. Milte C.M., Sinn N., Buckley J.D., et al. Polyunsaturated fatty acids, cognition and literacy in children with ADHD with and without learning difficulties. JChild Health Care 2011, 15(4):299-311.
117. Richardson A.J. Clinical trials of fatty acid treatment in ADHD, dyslexia, dyspraxia and the autistic spectrum. Prostaglandins Leukot Essent Fatty Acids 2004, 70:383-390.
118. Johnson M., Ostlund S., Fransson G., et al. Omega-3/omega-6 fatty acids for attention deficit hyperactivity disorder: a randomized placebo-controlled trial in children and adolescents. JAtten Disord 2009, 12:394-401.
119. Stevens L., Zhang W., Peck L., et al. EFA supplementation in children with inattention, hyperactivity, and other disruptive behaviors. Lipids 2003, 38:1007-1021.
120. Perera H., Jeewandara K.C., Seneviratne S., et al. Combined ω3 and ω6 supplementation in children with attention-deficit hyperactivity disorder (ADHD) refractory to methylphenidate treatment: a double-blind, placebo-controlled study. J Child Neurol 2012, 27(6):747-753.
121. Harding K.L., Judah R.D., Gant C. Outcome-based comparison of ritalin versus food-supplement treated children with AD/HD. Altern Med Rev 2003, 8:319-330.
122. Bloch M.H., Qawasmi A. Omega-3 fatty acid supplementation for the treatment of children with attention-deficit/hyperactivity disorder symptomatology: systematic review and meta-analysis. JAm Acad Child Adolesc Psychiatry 2011, 50:991-1000.
123. Swan G.E., Carmelli D., Rosenman R.H. Psychological characteristics in twins discordant for smoking behavior: a matched-twin-pair analysis. Addict Behav 1988, 13:51-60.
124. Gesch C.B., Hammond S.M., Hampson S.E., et al. Influence of supplementary vitamins, minerals and essential fatty acids on the antisocial behaviour of young adult prisoners. Randomised, placebo-controlled trial. Br J Psychiatry 2002, 181:22-28.
125. Corrigan F., Gray R., Strathdee A., et al. Fatty acid analysis of blood from violent offenders. JForensic Psychiatr Psychol 1994, 5:83-92.
126. Schoenthaler S.J. Diet and criminal behavior: a criminological evaluation of the Arlington, Virginia proceedings. Pers Individ Dif 1991, 12:339-340.
127. Schoenthaler S.J. The Alabama diet-behavior program: an evaluation at the Coosa Valley regional detention center. Pers Individ Dif 1991, 12:336.
128. Schoenthaler S.J., Bier I.D. The effect of vitamin-mineral supplementation on juvenile delinquency among American schoolchildren: a randomized, double-blind placebo-controlled trial. JAltern Complement Med 2000, 6:7-17.
129. Weller E.B., Weller R.A., Rooney M.T., et al. Children's interview for psychiatric syndromes (ChIPS) 1999, American Psychiatric Press, Inc, Arlington (VA).
130. Gow R.V., Vallee-Tourangeau F., Crawford M.A., et al. Omega-3 fatty acids are inversely related to callous and unemotional traits in adolescent boys with attention deficit hyperactivity disorder. Prostaglandins Leukot Essent Fatty Acids 2013, 88(6):411-418.
131. Frick P.J., Stickle T.R., Dandreaux D.M., et al. Callous-unemotional traits in predicting the severity and stability of conduct problems and delinquency. JAbnorm Child Psychol 2005, 33:471-487.
132. Frick P.J., White S.F. Research review: the importance of callous-unemotional traits for developmental models of aggressive and antisocial behavior. JChild Psychol Psychiatry 2008, 49:359-375.
133. Viding E. Annotation: understanding the development of psychopathy. JChild Psychol Psychiatry 2004, 45:1329-1337.
134. Viding E., Jones A.P., Frick P.J., et al. Heritability of antisocial behaviour at 9: do callous-unemotional traits matter?. Dev Sci 2008, 11:17-22.
135. Zaalberg A., Nijman H., Bulten E., et al. Effects of nutritional supplements on aggression, rule-breaking, and psychopathology among young adult prisoners. Aggress Behav 2010, 36:117-126.
136. Edwards R., Peet M., Shay J., et al. Omega-3 polyunsaturated fatty acid levels in the diet and in red blood cell membranes of depressed patients. JAffect Disord 1998, 48:149-155.
137. Peet M., Murphy B., Shay J., et al. Depletion of omega-3 fatty acid levels in red blood cell membranes of depressive patients. Biol Psychiatry 1998, 43:315-319.
138. Conklin S.M., Harris J.I., Manuck S.B., et al. Serum omega-3 fatty acids are associated with variation in mood, personality and behavior in hypercholesterolemic community volunteers. Psychiatry Res 2007, 152:1-10.
139. Conklin S.M., Manuck S.B., Yao J.K., et al. High omega-6 and low omega-3 fatty acids are associated with depressive symptoms and neuroticism. Psychosom Med 2007, 69:932-934.
140. Hibbeln J.R. Seafood consumption, the DHA content of mothers' milk and prevalence rates of postpartum depression: a cross-national, ecological analysis. JAffect Disord 2002, 69:15-29.
141. Hibbeln J.R. Fish consumption and major depression. Lancet 1998, 351:1213.
142. Noaghiul S., Hibbeln J.R. Cross-national comparisons of seafood consumption and rates of bipolar disorders. Am J Psychiatry 2003, 160:2222-2227.
143. Hibbeln J.R. Seafood consumption and homicide mortality. A cross-national ecological analysis. World Rev Nutr Diet 2001, 88:41-46.
144. Omega-3 fatty acid deficiency syndrome: opportunities for disease prevention 2013, Nova Science Pub Incorporated, Hauppauge (NY). R.K. McNamara (Ed.).
145. Ginsberg Y., Lindefors N. Methylphenidate treatment of adult male prison inmates with attention-deficit hyperactivity disorder: randomised double-blind placebo-controlled trial with open-label extension. Br J Psychiatry 2012, 200:68-73.
146. Jazayeri S., Tehrani-Doost M., Keshavarz S.A., et al. Comparison of therapeutic effects of omega-3 fatty acid eicosapentaenoic acid and fluoxetine, separately and in combination, in major depressive disorder. Aust N Z J Psychiatry 2008, 42:192-198.
147. Peet M., Horrobin D.F. Adose-ranging study of the effects of ethyl-eicosapentaenoate in patients with ongoing depression despite apparently adequate treatment with standard drugs. Arch Gen Psychiatry 2002, 59:913-919.
148. Freeman M.P., Hibbeln J.R., Wisner K.L., et al. Omega-3 fatty acids: evidence basis for treatment and future research in psychiatry. JClin Psychiatry 2006, 67:1954-1967.
149. Appleton K.M., Rogers P.J., Ness A.R. Updated systematic review and meta-analysis of the effects of n-3 long-chain polyunsaturated fatty acids on depressed mood. Am J Clin Nutr 2010, 91:757-770.
150. Kraguljac N.V., Montori V.M., Pavuluri M., et al. Efficacy of omega-3 fatty acids in mood disorders - a systematic review and metaanalysis. Psychopharmacol Bull 2009, 42:39-54.
151. Martins J.G. EPA but not DHA appears to be responsible for the efficacy of omega-3 long chain polyunsaturated fatty acid supplementation in depression: evidence from a meta-analysis of randomized controlled trials. JAm Coll Nutr 2009, 28:525-542.
152. Martins J.G., Bentsen H., Puri B.K. Eicosapentaenoic acid appears to be the key omega-3 fatty acid component associated with efficacy in major depressive disorder: a critique of Bloch and Hannestad and updated meta-analysis. Mol Psychiatry 2012, 17:1144-1149. [discussion: 1163-7].
153. Sublette M.E., Ellis S.P., Geant A.L., et al. Meta-analysis of the effects of eicosapentaenoic acid (EPA) in clinical trials in depression. JClin Psychiatry 2011, 72:1577-1584.
154. Lin P.Y., Mischoulon D., Freeman M.P., et al. Are omega-3 fatty acids antidepressants or just mood-improving agents? The effect depends upon diagnosis, supplement preparation, and severity of depression. Mol Psychiatry 2012, 17:1161-1163. [author reply: 1163-7].
155. Bloch M.H., Hannestad J. Omega-3 fatty acids for the treatment of depression: systematic review and meta-analysis. Mol Psychiatry 2012, 17:1272-1282.
156. Kirsch I., Deacon B.J., Huedo-Medina T.B., et al. Initial severity and antidepressant benefits: a meta-analysis of data submitted to the Food and Drug Administration. PLoS Med 2008, 5:e45.
157. Hibbeln J.R. Depression, suicide and deficiencies of omega-3 essential fatty acids in modern diets. World Rev Nutr Diet 2009, 99:17-30.
158. Lewis M.D., Hibbeln J.R., Johnson J.E., et al. Suicide deaths of active-duty US military and omega-3 fatty-acid status: a case-control comparison. JClin Psychiatry 2011, 72:1585-1590.
159. Sublette M.E., Hibbeln J.R., Galfalvy H., et al. Omega-3 polyunsaturated essential fatty acid status as a predictor of future suicide risk. Am J Psychiatry 2006, 163:1100-1102.
160. Levin E.D., McClernon F.J., Rezvani A.H. Nicotinic effects on cognitive function: behavioral characterization, pharmacological specification, and anatomic localization. Psychopharmacology 2006, 184:523-539.
161. Huan M., Hamazaki K., Sun Y., et al. Suicide attempt and n-3 fatty acid levels in red blood cells: a case control study in China. Biol Psychiatry 2004, 56:490-496.
162. Amminger G.P., Schafer M.R., Papageorgiou K., et al. Long-chain omega-3 fatty acids for indicated prevention of psychotic disorders: a randomized, placebo-controlled trial. Arch Gen Psychiatry 2010, 67:146-154.
163. Itomura M., Hamazaki K., Sawazaki S., et al. The effect of fish oil on physical aggression in schoolchildren-a randomized, double-blind, placebo-controlled trial. JNutr Biochem 2005, 16:163-171.
164. Hamazaki K., Syafruddin D., Tunru I.S., et al. The effects of docosahexaenoic acid-rich fish oil on behavior, school attendance rate and malaria infection in school children-a double-blind, randomized, placebo-controlled trial in Lampung, Indonesia. Asia Pac J Clin Nutr 2008, 17:258-263.
165. Ramsden C.E., Mann J.D., Faurot K.R., et al. Low omega-6 vs. low omega-6 plus high omega-3 dietary intervention for chronic daily headache: protocol for a randomized clinical trial. Trials 2011, 12:97.
166. Freeman M.P. Omega-3 fatty acids and perinatal depression: a review of the literature and recommendations for future research. Prostaglandins Leukot Essent Fatty Acids 2006, 75:291-297.
167. Carmelli D., Swan G.E., Robinette D., et al. Genetic influence on smoking-a study of male twins. NEngl J Med 1992, 327:829-833.