Smoking, gender, and dietary influences on erythrocyte essential fatty acid composition among patients with schizophrenia or schizoaffective disorder

Biological Psychiatry

Volumn 53, Issue 5, 2003, Pages 431-441

  Hibbeln, Joseph R ^a   Makino, Kevin K ^a   Martin, Catherine E ^b   Dickerson, Faith ^c   Boronow, John ^c   Fenton, Wayne S ^b  

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

^b NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^c SHEPPARD PRATT HEALTH SYSTEM   (United States)

Author keywords

Arachidonic acid; Docosahexaenoic acid; Eicosapentaenoic acid; Omega 3 fatty acids; Schizophrenia; Smoking

Indexed keywords

ARACHIDONIC ACID; DOCOSAHEXAENOIC ACID; ESSENTIAL FATTY ACID; ICOSAPENTAENOIC ACID; ICOSAPENTAENOIC ACID ETHYL ESTER; LINOLENIC ACID;

ADULT; ARTICLE; ARTIFACT; CELL COMPOSITION; CONTROLLED STUDY; DIET SUPPLEMENTATION; DISEASE SEVERITY; ERYTHROCYTE; FATTY ACID ANALYSIS; FATTY ACID METABOLISM; FEMALE; HUMAN; HUMAN CELL; LIPID DIET; MAJOR CLINICAL STUDY; MALE; METABOLIC DISORDER; MULTIVARIATE ANALYSIS; PREDICTION; PRIORITY JOURNAL; RATING SCALE; SCHIZOAFFECTIVE PSYCHOSIS; SCHIZOPHRENIA; SEX DIFFERENCE; SMOKING;

EID: 0037373583     PISSN: 00063223     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3223(02)01549-4     Document Type: Article

References (90)

1. 2 activity in serum of neuroleptic-naive psychiatric inpatients. Pharmacopsychiatry. 26:1993;94-98.
2. Assies J., Lieverse R., Vreken P., Wanders R.J., Dingemans P.M., Linszen D.H. Significantly reduced docosahexaenoic and docosapentaenoic acid concentrations in erythrocyte membranes from schizophrenic patients compared with a carefully matched control group. Biol Psychiatry. 6:2001;510-522.
3. Beckman J.K., Borowitz S.M., Burr I.M. The role of phospholipase A activity in rat liver microsomal lipid peroxidation. J Biol Chem. 262:1987;1479-1484.
4. 2 activity in Epstein-Barr virus-transformed lymphoblast cells from schizophrenic patients. Biol Psychiatry. 29:1991;1058-1062.
5. Craig W.Y., Palomaki G.E., Haddow J.E. Cigarette smoking and serum lipid and lipoprotein concentrations An analysis of published data . BMJ. 298:1989;784-788.
6. D'Avanzo B., La Vecchia C., Braga C., Franceschi S., Negri E., Parpinel M. Nutrient intake according to education, smoking, and alcohol in Italian women. Nutr Cancer. 28:1997;46-51.
7. Deicken R.F., Calabrese G., Merrin E.L., Meyerhoff D.J., Dillon W.P., Weiner M.W., et al. 31phosphorus magnetic resonance spectroscopy of the frontal and parietal lobes in chronic schizophrenia. Biol Psychiatry. 36:1994;503-510.
8. Deicken R.F., Calabrese G., Merrin E.L., Vinogradov S., Fein G., Weiner M.W. Asymmetry of temporal lobe phosphorous metabolism in schizophrenia A 31phosphorous magnetic resonance spectroscopic imaging study . Biol Psychiatry. 38:1995;279-286.
9. Substances affirmed as generally recognized as safe Menhaden oil . Federal Register. 62:1997;30751-30757.
10. Diwan A., Castine M., Pomerleau C.S., Meador-Woodruff J.H., Dalack G.W. Differential prevalence of cigarette smoking in patients with schizophrenic vs. mood disorders. Schizophr Res. 1-2:1998;113-118.
11. 2 and schizophrenia. Schizophr Res. 31:1998;185-196.
12. Fenton W.S., Dickerson F., Boronow J., Hibbeln J.R., Knable M. A placebo-controlled trial of omega-3 fatty acid (ethyl-EPA) supplementation for residual symptoms and cognitive impairment in schizophrenia. Am J Psychiatry. 158:2001;2071-2074.
13. Fenton W.S., Hibbeln J.R., Knable M. Essential fatty acids, lipid membrane abnormalities, and the diagnosis and treatment of schizophrenia. Biol Psychiatry. 47:2000;8-21.
14. Fujimoto T., Nakano T., Takano T., Hokazono Y., Asakura T., Tsuji T. Study of chronic schizophrenic patients using 31P magnetic resonance chemical shift imaging. Acta Psychiatr Scand. 86:1992;455-462.
15. Fukuzako H., Fukuzako T., Hashiguchi T., Kodama S., Takigawa M., Fujimoto T. Changes in levels of phosphorus metabolites in temporal lobes of drug-naive schizophrenic patients. Am J Psychiatry. 156:1999;1205-1208.
16. Fukuzako H., Fukuzako T., Kodama S., Fujimoto T., Takigawa M. Haloperidol improves membrane phospholipid abnormalities in temporal lobes of schizophrenic patients. Neuropsychopharmacology. 21:1999;542-549.
17. Fukuzako H., Fukuzako T., Takeuchi K., Ohbo Y., Ueyama K., Takigawa M., et al. Phosphorus magnetic resonance spectroscopy in schizophrenia Correlation between membrane phospholipid metabolism in the temporal lobe and positive symptoms . Prog Neuropsychopharmacol Biol Psychiatry. 20:1996;629-640.
18. 2 and the hypofrontality hypothesis of schizophrenia. Prostaglandins Leukot Essent Fatty Acids. 55:1996;109-113.
19. 2 activity in schizophrenia A replication study . Biol Psychiatry. 28:1990;495-501.
20. 2 activity in schizophrenic patients Reduction after neuroleptic therapy . Biol Psychiatry. 22:1987;421-426.
21. Glen A.I., Glen E.M., Horrobin D.F., Vaddadi K.S., Spellman M., Morse-Fisher N., et al. A red cell membrane abnormality in a subgroup of schizophrenic patients Evidence for two diseases . Schizophr Res. 12:1994;53-61.
22. Grimsgaard S., Bonaa K.H., Hansen J.B., Myhre E.S. Effects of highly purified eicosapentaenoic acid and docosahexaenoic acid on hemodynamics in humans. Am J Clin Nutr. 68:1998;52-59.
23. Grimsgaard S., Bonaa K.H., Hansen J.B., Nordoy A. Highly purified eicosapentaenoic acid and docosahexaenoic acid in humans have similar triacylglycerol-lowering effects but divergent effects on serum fatty acids. Am J Clin Nutr. 66:1997;649-659.
24. Hinsberger A.D., Williamson P.C., Carr T.J., Stanley J.A., Drost D.J., Densmore M., et al. Magnetic resonance imaging volumetric and phosphorus 31 magnetic resonance spectroscopy measurements in schizophrenia. J Psychiatry Neurosci. 22:1997;111-117.
25. Hirai A, Terano T, Saito H, Tamura Y (1989): Omega-3 fatty acids: Epidemiological and clinical aspects. In: Spiller GA, Scala J, editors. New Protective Roles for Selected Nutrients. New York: Alan R. Liss Inc., pp 229-252.
26. Horrobin D. The lipid hypothesis of schizophrenia. Skinner E.R. Brain Lipids and Disorders in Biological Psychiatry. 2002;39-49 Elsevier, New York.
27. Horrobin D.F. The membrane phospholipid hypothesis as a biochemical basis for the neurodevelopmental concept of schizophrenia. Schizophr Res. 30:1998;193-208.
28. Horrobin D.F., Manku M.S., Morse-Fisher N., Vaddadi K.S., Courtney P., Glen A.I., et al. Essential fatty acids in plasma phospholipids in schizophrenic patients. Biol Psychiatry. 25:1989;562-568.
29. Hunter D.J., Rimm E.B., Sacks F.M., Stampfer M.J., Colditz G.A., Litin L.B., et al. Comparison of measures of fatty acid intake by subcutaneous fat aspirate, food frequency questionnaire, and diet records in a free-living population of US men. Am J Epidemiol. 135:1992;418-427.
30. 2 activity between acute psychiatric patients and controls. Schizophr Res. 26:1997;103-105.
31. Kato T., Shioiri T., Murashita J., Hamakawa H., Inubushi T., Takahashi S. Lateralized abnormality of high-energy phosphate and bilateral reduction of phosphomonoester measured by phosphorus-31 magnetic resonance spectroscopy of the frontal lobes in schizophrenia. Psychiatry Res. 61:1995;151-160.
32. Kay S.R., Fiszbein A., Opler L.A. The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr Bull. 13:1987;261-276.
33. Keshavan M.S., Sanders R.D., Pettegrew J.W., Dombrowsky S.M., Panchalingam K.S. Frontal lobe metabolism and cerebral morphology in schizophrenia 31P MRS and MRI studies . Schizophr Res. 10:1993;241-246.
34. Komoroski R.A., Pearce J.M., Griffin W.S., Mrak R.E., Omori M., Karson C.N. Phospholipid abnormalities in postmortem schizophrenic brains detected by 31P nuclear magnetic resonance spectroscopy A preliminary study . Psychiatry Res. 106:2001;171-180.
35. Koo L.C. Diet and lung cancer 20+ years later More questions than answers? Int J Cancer. 10:1997;22-29.
36. Lehman A.F., Steinwachs D.M. Translating research into practice The Schizophrenia Patient Outcomes Research Team (PORT) treatment recommendations . Schizophr Bull. 24:1998;1-10.
37. Lohr B., Flynn K. Smoking and schizophrenia. Schizophr Res. 8:1992;93-102.
38. London S.J., Sacks F.M., Caesar J., Stampfer M.J., Siguel E., Willett W.C. Fatty acid composition of subcutaenous adipose tissue and diet in postmenopausal women. Am J Epidemiol. 54:1991;340-345.
39. Mahadick S., Evans D., Lal H. Oxidative stress and role of antioxidant and ω-3 essential fatty acid supplementation in schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry. 25:2001;463-493.
40. 2. J Pharmacol Exp Ther. 280:1997;1277-1283.
41. Mellor J.E., Laugharne J.D., Peet M. Schizophrenia symptoms and dietary intake of n-3 fatty acids. Schizophr Res. 18:1995;85-86.
42. Montgomery S.A., Asberg M. A new depression scale designed to be sensitive to change. Br J Psychiatry. 134:1979;382-389.
43. Mori T.A., Bao D.Q., Burke V., Puddey I.B., Beilin L.J. Docosahexaenoic acid but not eicosapentaenoic acid lowers ambulatory blood pressure and heart rate in humans. Hypertension. 34:1999;253-260.
44. Moriguchi T., Greiner R.S., Salem N. Jr. Behavioral deficits associated with dietary induction of decreased brain docosahexaenoic acid concentration. J Neurochem. 75:2000;2563-2573.
45. Morrison W.R., Smith L.M. Preparation of fatty acid methyl esters and dimethylacetals with boron-fluoride methanol. J Lipid Res. 5:1959;600-608.
46. Morrow J.D., Frei B., Longmire A.W., Gaziano J.M., Lynch S.M., Shyr Y., et al. Increase in circulating products of lipid peroxidation (F2-isoprostanes) in smokers. Smoking as a cause of oxidative damage. N Eng J Med. 332:1995;1198-1203.
47. National Institutes of Mental Health (1976): ECDEU Assessment Manual for Psychopharmacology. In: Guy W, editor. Washington, DC: U.S. Department of Health Education and Welfare.
48. CGI (Clinical Global Impression) Scale. Psychopharmacology Bulletin. 21:1985;839-840.
49. Nigam S., Schewe T. Phospholipase A(2)s and lipid peroxidation. Biochim Biophys Acta. 1488:2000;167-181.
50. 2 activity in schizophrenic patients and other psychiatric patients. Biol Psychiatry. 34:1993;641-649.
51. O'Callaghan E., Redmond O., Ennis R., Stack J., Kinsella A., Ennis J.T., et al. Initial investigation of the left temporoparietal region in schizophrenia by 31P magnetic resonance spectroscopy. Biol Psychiatry. 29:1991;1149-1152.
52. Pangerl A.M., Steudle A., Jaroni H.W., Rufer R., Gattaz W.F. Increased platelet membrane lysophosphatidylcholine in schizophrenia. Biol Psychiatry. 30:1991;837-840.
53. Pawlosky R.J., Salem N.J.r. Alcohol consumption in rhesus monkeys depletes tissues of polyunsaturated fatty acids and alters essential fatty acid metabolism. Alcohol Clin Exp Res. 23:1999;311-317.
54. Peet M., Brind J., Ramchand C.N., Shah S., Vankar G.K. Two double-blind placebo-controlled pilot studies of eicosapentaenoic acid in the treatment of schizophrenia. Schizophr Res. 49:2001;243-251.
55. Peet M., Glen I., Horrobin D. Phospholipid Spectrum Disorder in Psychiatry. 1999;Marius Press, Lancashire, UK.
56. Peet M., Laugharne J., Rangarajan N., Horrobin D., Reynolds G. Depleted red cell membrane essential fatty acids in drug-treated schizophrenic patients. J Psychiatr Res. 29:1995;227-232.
57. Peet M., Laugharne J.D., Horrobin D.F., Reynolds G.P. Arachidonic acid A common link in the biology of schizophrenia? Arch Gen Psychiatry. 51:1994;665-666.
58. Peet M., Laugharne J.D.E., Mellor J., Ramchand C.N. Essential fatty acid deficiency in erythrocyte membranes from chronic schizophrenic patients and the clinical effects of dietary supplementation. Prostaglandins Leukot Essent Fatty Acids. 55:1996;71-75.
59. 2 gene with schizophrenia. Psychiatr Genet. 8:1998;191-192.
60. Pettegrew J.W., Keshavan M.S., Minshew N.J. 31P nuclear magnetic resonance spectroscopy Neurodevelopment and schizophrenia . Schizophr Bull. 19:1993;35-53.
61. Pettegrew J.W., Keshavan M.S., Panchalingam K., Strychor S., Kaplan D.B., Tretta M.G., et al. Alterations in brain high-energy phosphate and membrane phospholipid metabolism in first-episode, drug-naive schizophrenic patients. A pilot study of the dorsal prefrontal cortex by in vivo phosphorus 31 nuclear magnetic resonance spectroscopy. Arch Gen Psychiatry. 48:1991;563-568.
62. Porter N.A. Chemistry of lipid peroxidation. Methods Enzymol. 105:1984;273-282.
63. Pryor W.A. Cigarette smoke radicals and the role of free radicals in chemical carcinogenicity. Environ Health Perspect. 105:1997;875-882.
64. Puri B.K., Richardson A.J. Sustained remission of positive and negative symptoms of schizophrenia following treatment with eicosapentaenoic acid. Arch Gen Psychiatry. 55:1998;188-189.
65. Puri B.K., Richardson A.J., Horrobin D.F., Easton T., Saeed N., Oatridge A., et al. Eicosapentaenoic acid treatment in schizophrenia associated with symptom remission, normalisation of bloody fatty acids, reduced neuronal membrane phospholipid turnover and structural brain changes. Int J Clin Pract. 54:2000;57-63.
66. Randolph C. RBANS Manual-Repeatable Battery for the Assessment of Neuropsychological Status. 1998;Psychological Corp. (Harcourt), San Antonio, TX.
67. Rapoport S.I., Chang M.C., Spector A.A. Delivery and turnover of plasma-derived essential PUFAs in mammalian brain. J Lipid Res. 42:(5):2001;678-685.
68. Romon M., Nuttens M.C., Theret N., Delbart C., Lecerf J.M., Fruchart J.C., et al. Comparison between fat intake assessed by a 3-day food record and phospholipid fatty acid composition of red blood cells Results from the Monitoring of Cardiovascular Disease-Lille Study . Metabolism. 44:1995;1139-1145.
69. 2. Arch Gen Psychiatry. 54:1997;487-494.
70. 2 activities in brain of patients with schizophrenia. Brain Res. 821:1999;407-413.
71. Rotrosen J., Wolkin A. Phospholipid and prostaglandin hypotheses of schizophrenia. Meltzer H. Psychopharmacology The Third Generation of Progress . 1987;759-764 Raven Press, New York.
72. Sastry B.V., Chance M.B., Hemontolor M.E., Goddijn-Wessel T.A. Formation and retention of cotinine during placental transfer of nicotine in human placental cotyledon. Pharmacology. 57:1998;104-116.
73. 2 and its significance to macular function. J Ocul Pharmacol Ther. 14:1998;447-458.
74. Shioiri T., Hamakawa H., Kato T., Fujii K., Murashita J., Inubushi T., et al. Frontal lobe membrane phospholipid metabolism and ventricle to brain ratio in schizophrenia Preliminary 31P-MRS and CT studies . Eur Arch Psychiatry Clin Neurosci. 250:2000;169-174.
75. Simon J.A., Fong J., Bernert J.T. Jr, Browner W.S. Relation of smoking and alcohol consumption to serum fatty acids. Am J Epidemiol. 144:1996;325-334.
76. Simpson G.M., Angus J.W. A rating scale for extrapyramidal side effects. Acta Psychiatr Scand Suppl. 212:1970;11-19.
77. Stanley J.A., Williamson P.C., Drost D.J., Carr T.J., Rylett R.J., Morrison-Stewart S., et al. Membrane phospholipid metabolism and schizophrenia An in vivo 31P-MR spectroscopy study . Schizophr Res. 13:1994;209-215.
78. Stanley J.A., Williamson P.C., Drost D.J., Carr T.J., Rylett R.J., Malla A., et al. An in vivo study of the prefrontal cortex of schizophrenic patients at different stages of illness via phosphorus magnetic resonance spectroscopy. Arch Gen Psychiatry. 52:1995;399-406.
79. Talmud P.J., Humphries S.E. Genetic polymorphisms, lipoproteins and coronary artery disease risk. Curr Opin Lipidol. 12:2001;405-409.
80. Thompson R.L., Pyke S.D., Scott E.A., Thompson S.G., Wood D.A. Dietary change after smoking cessation A prospective study . Br J Nutr. 74:1995;27-38.
81. Vaddadi K.S., Courtney P., Gilleard C.J., Manku M.S., Horrobin D.F. A double blind trial of essential fatty acid supplementation in patients with tradive dyskinesia. Psychiatry Res. 27:1989;313-323.
82. Vaddadi K.S., Gilleard C.J., Mindham R.H.S., Butler R. A controlled trial of prostaglandin E1 precursor in chronic neuroleptic resistant schizophrenic patients. Psychopharmacology. 88:1986;362-367.
83. Vaddadi K.S., Gilleard C.J., Soosai E., Polonowita A.K., Gibson R.A., Burrows G.D. Schizophrenia, tardive dyskinesia and essential fatty acids. Schizophr Res. 20:1996;287-294.
84. Volz H.P., Riehemann S., Maurer I., Smesny S., Sommer M., Rzanny R., et al. Reduced phosphodiesters and high-energy phosphates in the frontal lobe of schizophrenic patients A (31)P chemical shift spectroscopic-imaging study . Biol Psychiatry. 47:2000;954-961.
85. Volz H.P., Rossger G., Riehemann S., Hubner G., Maurer I., Wenda B., et al. Increase of phosphodiesters during neuroleptic treatment of schizophrenic patients A longitudinal 31P-magnetic resonance spectroscopic study . Biol Psychiatry. 45:1999;1221-1225.
86. von Schacky C., Weber P.C. Metabolism and effects on platelet function of the purified eicosapentaenoic and docosahexaenoic acids in humans. J Clin Invest. 76:1985;2446-2450.
87. Willett W.C., Sampson L., Stampfer M.J., Rosner B., Bain C., Witschi J., et al. Reproducibility and validity of a semiquantitative food frequency questionnaire. Am J Epidemiol. 122:1985;51-65.
88. Yao J.K., Leonard S., Reddy R.D. Membrane phospholipid abnormalities in postmortem brains from schizophrenic patients. Schizophr Res. 42:2000;7-17.
89. Yao J.K., van Kammen D.P., Gurklis J. Red blood cell membrane dynamics in schizophrenia. III. Correlation of fatty acid abnormalities with clinical measures. Schizophr Res. 13:1994;227-232.
90. Yao J.K., van Kammen D.P., Welker J.A. Red blood cell membrane dynamics in schizophrenia. II. Fatty acid composition. Schizophr Res. 13:1994;217-226.