Oxidative stress-related biomarkers in autism: Systematic review and meta-analyses

Free Radical Biology and Medicine

Volumn 52, Issue 10, 2012, Pages 2128-2141

  Frustaci, Alessandra ^a   Neri, Monica ^a   Cesario, Alfredo ^a,b   Adams, James B ^c   Domenici, Enrico ^d   Dalla Bernardina, Bernardo ^e   Bonassi, Stefano ^a  

^a IRCCS SAN RAFFAELE PISANA   (Italy)

^b CATHOLIC UNIVERSITY   (Italy)

^c Arizona State University   (United States)

^d F HOFFMANN LA ROCHE LTD   (Switzerland)

^e UNIVERSITY OF VERONA   (Italy)

Author keywords

Amino acids; Antioxidants; Autistic disorder; Biological markers; Case control studies; Free radicals; Genetic polymorphisms; Glutathione; Oxidative stress; Oxidoreductases; Vitamins

Indexed keywords

5,10 METHYLENETETRAHYDROFOLATE REDUCTASE (FADH2); ALPHA TOCOPHEROL; ASCORBIC ACID; BIOLOGICAL MARKER; CATALASE; CERULOPLASMIN; CYANOCOBALAMIN; CYSTATHIONINE; CYSTEINE; CYSTEINYLGLYCINE; FOLIC ACID; GLUTATHIONE; GLUTATHIONE PEROXIDASE; HOMOCYSTEINE; METHIONINE; NITRIC OXIDE; PYRIDOXINE; RETINOL; SUPEROXIDE DISMUTASE; THIOBARBITURIC ACID REACTIVE SUBSTANCE; VITAMIN D;

AUTISM; COMPARATIVE STUDY; DISEASE ASSOCIATION; DISEASE COURSE; ENZYME BLOOD LEVEL; HUMAN; META ANALYSIS; OXIDATIVE STRESS; PRIORITY JOURNAL; REVIEW; SYSTEMATIC REVIEW; VITAMIN BLOOD LEVEL;

BIOLOGICAL MARKERS; CHILD; CHILD DEVELOPMENT DISORDERS, PERVASIVE; CHILD, PRESCHOOL; GLUTATHIONE; HUMANS; METHYLENETETRAHYDROFOLATE REDUCTASE (NADPH2); OXIDATIVE STRESS; VITAMINS;

EID: 84861035734     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2012.03.011     Document Type: Review

References (103)

1. American Psychiatric Association Diagnostic and Statistical Manual of Mental Disorders. 4th ed. Washington, DC: American Psychiatric Association; 2000. (text revised).
2. Rice, C. Prevalence of autism spectrum disorders - autism and developmental disabilitiesmonitoring network, United States, 2006. MMWR 58(SS10): 1-20; 2009.
3. Myers, S. M. The status of pharmacotherapy for autism spectrum disorders. Expert Opin Pharmacother 8:1579-1603; 2007.
4. Leskovec, T. J.; Rowles, B. M.; Finding, R. L. Pharmacological treatment options for autism spectrum disorders in children and adolescents. Harvard Rev Psychiatry 16:97-112; 2008.
5. Rogers, S. J.; Vismara, L. A. Evidence-based comprehensive treatments for early autism. J Clin Child Adolesc Psychol 37:8-38; 2008.
6. Schumann, C. M.; Bloss, C. S.; Barnes, C. C.; Wideman, G. M.; Carper, R. A.; Akshoomoff, N.; Pierce, K.; Hagler, D.; Schork, N.; Lord, C.; Courchesne, E. Longitudinal magnetic resonance imaging study of cortical development through early childhood in autism. J Neurosci 30:4419-4427; 2010.
7. Stoltenberg, C.; Schjølberg, S.; Bresnahan, M.; Hornig, M.; Hirtz, D.; Dahl, C.; Lie, K. K.; Reichborn-Kjennerud, T.; Schreuder, P.; Alsaker, E.; Øyen, A. S.; Magnus, P.; Surén, P.; Susser, E.; Lipkin, W. I.; ABC Study Group The autism birth cohort: a paradigm for gene-environment-timing research. Mol Psychiatry 15:676-680; 2010.
8. Pierce, K.; Glatt, S. J.; Liptak, G. S.; McIntyre, L. L. The power and promise of identifying autism early: insights from the search for clinical and biological markers. Ann Clin Psychiatry 21:132-147; 2009.
9. Theoharides, T. C.; Kempuraj, D.; Redwood, L. Autism: an emerging neuroimmune disorder in search of therapy. Expert Opin Pharmacother 10:2127-2143; 2009.
10. Fombonne, E.; Zakarian, R.; Bennett, A.; Meng, L.; McLean-Heywood, D. Pervasive developmental disorders in Montreal, Quebec, Canada: prevalence and links with immunizations. Pediatrics 118:139-150; 2006.
11. Hertz-Picciotto, I.; Delwiche, L. The rise in autism and the role of age at diagnosis. Epidemiology 20:84-90; 2009.
12. Herbert, M. R. Contributions of the environment and environmentally vulnerable physiology to autism spectrum disorders. Curr Opin Neurol 23:103-110; 2010.
13. Nunomura, A.; Moreira, P. I.; Lee, H. G.; Zhu, X.; Castellani, R. J.; Smith, M. A.; Perry, G. Neuronal death and survival under oxidative stress in Alzheimer and Parkinson diseases. CNS Neurol Disord Drug Targets 6:411-423; 2007.
14. Gerhardsson, L.; Blennow, K.; Lundh, T.; Londos, E.; Minthon, L. Concentrations of metals, b-amyloid and tau-markers in cerebrospinal fluid in patients with Alzheimer's disease. Dement Geriatr Cognit Disord 28:88-94; 2009.
15. Valko, M.; Morris, H.; Cronin, M. T. Metals, toxicity and oxidative stress. Curr Med Chem 12:1161-1208; 2005.
16. Deth, R.; Muratore, C.; Benzecry, J.; Power-Charnitsky, V. -A.; Waly, M. How environmental and genetic factors combine to cause autism: a redox/methylation hypothesis. Neurotoxicology 29:190-201; 2008.
17. Campagnoni, A. T. Molecular biology of myelin proteins from the central nervous system. J Neurochem 51:1-14; 1988.
18. Rawal, N.; Lee, Y. J.; Paik, W. K.; Kim, S. Studies on NG-methylarginine derivatives in myelin basic protein from developing and mutant mouse brain. Biochem J 287:929-935; 1992.
19. Persico, A. M.; Bourgeron, T. Searching for ways out of the autism maze: genetic, epigenetic and environmental clues. Trends Neurosci 29:349-358; 2006.
20. Abrahams, B. S.; Geschwind, D. H. Advances in autism genetics: on the threshold of a new neurobiology. Nat Rev Genet 9:341-355; 2008.
21. Abrahams, B. S.; Geschwind, D. H. Connecting genes to brain in the autism spectrum disorders. Arch Neurol 67:395-399; 2010.
22. McGinnis, W. R. Oxidative stress in autism. Alternat Ther 10:22-36; 2004.
23. Frossi, B.; de Carli, M.; Daniel, K. C.; Rivera, J.; Pupillo, C. Oxidative stress stimulates IL-4 and IL-6 production in mast cells by APE/Ref-1-dependent pathway. Eur J Immunol 33:2168-2177; 2003.
24. Halliwell, B. Oxidative stress and neurodegeneration: where are we now? J Neurochem 97:1634-1658; 2006.
25. Abdel-Salam, O. M. E.; Khadrawy, Y. A.; Salem, N. A.; Sleem, A. A. Oxidative stress in a model of toxic demyelination in rat brain: the effect of piracetam and vinpocetine. Neurochem Res 36:1062-1072; 2011.
26. Perluigi, M.; Di Domenico, F.; Goorgi, A.; Schinná, M. E.; Coccia, R.; Cini, C.; Bellia, F.; Cambria, M. T.; Cornelius, C.; Butterfield, D. A.; Calabrese, V. Redox proteomics in aging rat brain: involvement of mitochondrial reduced glutathione status and mitochondrial protein oxidation in the aging process. J Neurosci Res 88:3498-3507; 2010.
27. Spencer, W. A.; Jeyabalan, J.; Kichambre, S.; Gupta, R. C. Oxidatively generated DNA damage after Cu(II) catalysis of dopamine and related catecholamine neurotransmitters and neurotoxins: role of reactive oxygen species. Free Radic Biol Med 50:139-147; 2011.
28. Andreazza, A. C.; Kauer-Sant'Anna, M.; Frey, B. N.; Bond, D. J.; Kapczinski, F.; Young, L. T.; Yatham, L. N. Oxidative stress markers in bipolar disorder: a meta-analysis. J Affect Disord 111:135-144; 2008.
29. Ng, F.; Berk, M.; Dean, O.; Bush, A. I. Oxidative stress in psychiatric disorders: evidence base and therapeutic implications. Int J Neuropsycho-pharmacol 11:851-876; 2008.
30. Tsaluchidu, S.; Cocchi, M.; Tonello, L.; Puri, B. K. Fatty acids and oxidative stress in psychiatric disorders. BMC Psychiatry 8(Suppl. 1):S1-S5; 2008.
31. Sultana, R.; Perluigi, M.; Butterfield, D. A. Protein oxidation and lipid peroxidation in brain of subjects with Alzheimer's disease: insight into mechanism of neurodegeneration from redox proteomics. Antioxid Redox Signaling 8:2021-2037; 2010.
32. Evans, T. A.; Siedlak, S. A.; Lu, L.; Fu, X.; Wang, Z.; McGinnis, W. R.; Fakhoury, E.; Castellani, R. J.; Hazen, S. L.;Walsh,W. J.; Lewis, A. T.; Salomon, R. G.; Smith, M. A.; Perry, G.; Zhu, X. The autistic phenotype exhibits a remarkably localized modification of brain protein by products of free radical-induced lipid oxidation. Am J Biochem Biotechnol 4:61-72; 2008.
33. Chauhan, A.; Gu, F.; Essa, M. M.; Wegiel, J.; Kaur, K.; Brown, W. T.; Chauhan, V. Brain region-specific deficit in mitochondrial electron transport chain complexes in children with autism. J Neurochem 117:209-220; 2011.
34. Sajdel-Sulkowska, E. M.; Lipinski, B.; Windom, H.; Audhya, T.; McGinnis, W. Oxidative stress in autism: elevated cerebellar 3-nitrotyrosine levels. Am J Biochem Biotechnol 4:73-84; 2008.
35. Sajdel-Sulkowska, E. M.; Xu, M.; Koibuchi, N. Increase in cerebellar neurotrophin-3 and oxidative stress markers in autism. Cerebellum 8:366-372; 2009.
36. Sajdel-Sulkowska, E. M.; Xu, M.; McGinnis, W.; Koibuchi, N. Brain region-specific changes in oxidative stress and neurotrophin levels in autism spectrum disorders (ASD). Cerebellum 10:43-48; 2011.
37. Rossignol, D. A.; Frye, R. E. Mitochondrial dysfunction in autism spectrum disorders: a systematic review and meta-analysis. Mol Psychiatry 17:290-314; 2012.
38. Bradstreet, J. J.; Smith, S.; Baral, M.; Rossignol, D. A. Biomarker-guided interventions of clinically relevant conditions associated with autism spectrum disorders and attention deficit hyperactivity disorder. Alternat Med Rev 15:15-32; 2010.
39. Geier, D. A.; Geier, M. R. Autism spectrum disorder-associated biomarkers for case evaluation and management by clinical geneticists. Expert Rev Mol Diagn 8:671-674; 2008.
40. Ugolini, D.; Neri, M.; Casilli, C.; Bonassi, S. Development of search filters for retrieval of literature on the molecular epidemiology of cancer. Mutat Res 701:107-110; 2010.
41. Pas-ca, S. P.; Dronca, E.; Kaucsár, T.; Cřaciun, E. C.; Endreffy, E.; Ferencz, B. K.; Iftene, F.; Benga, I.; Cornean, R.; Banerjee, R.; Dronca, M. One carbon metabolism disturbances and the C677T MTHFR gene polymorphism in children with autism spectrum disorders. J Cell Mol Med 10:4229-4238; 2009.
42. Dronca, M.; Cřaciun, E. C.; Pas-ca, S. P.; Ftene, F. Antioxidant protection in autism. Ann West Univ Timisoara Ser Chem 16:169-174; 2007.
43. American Psychiatric Association Diagnostic and Statistical Manual of Mental Disorders.4th edition Washington, DC: American Psychiatric Association; 1994.
44. Schopler, E.; Reichler, R. J.; DeVellis, R. F.; Daly, K. Toward objective classification of childhood autism: Childhood Autism Rating Scale (CARS). J Autism Dev Disord 10:91-103; 1980.
45. American Psychiatric Association Diagnostic and Statistical Manual of Mental Disorders.3rd edition Washington, DC: American Psychiatric Association; 1980.
46. American Psychiatric Association Diagnostic and Statistical Manual of Mental Disorders.3rd edition Washington, DC: American Psychiatric Assoc; 1987. (revised).
47. Adams, J. B.; Audhya, T.; McDonough-Means, S.; Rubin, R. A.; Quig, D.; Geis, E.; Gehn, E.; Loresto, M.; Mitchell, J.; Atwood, S.; Barnhouse, S.; Lee, W. Nutritional and metabolic status of children with autism vs. neurotypical children, and the association with autism severity. Nutr Metab (London) 8:34; 2011.
48. Melnyk, S.; Fuchs, G. J.; Schulz, E.; Lopez, M.; Kahler, S. G.; Fussell, J. J.; Bellando, J.; Pavliv, O.; Rose, S.; Seidel, L.; Gaylor, D. W.; James, J. S. Metabolic imbalance associated with methylation dysregulation and oxidative damage in children with autism. J Autism Dev Disord 42:367-377; 2012.
49. Vergani, L.; Lanza, C.; Rivaro, P.; Abelmoschi, M. L.; Genti, S.; Veneselli, E.; Minniti, G.; Grasselli, E.; Canesi, L.; Voci, A. Metals, metallothioneins and oxidative stress in blood of autistic children. Res Autism Spectrum Disord 5:286-293; 2011.
50. Meguid, N. A.; Dardir, A. A.; Abdel-Raouf, E. R.; Hashish, A. Evaluation of oxidative stress in autism: defective antioxidant enzymes and increased lipid peroxidation. Biol Trace Elem Res 143:58-65; 2011.
51. Meguid, N. A.; Hashish, A. F.; Anwar, M.; Sidhom, G. Reduced serum levels of 25-hydroxy and 1,25-dihydroxy vitamin D in Egyptian children with autism. J Alternat Complement Med 16:641-645; 2010.
52. Mostafa, G. A.; El-Hadidi, E. S.; Hewedi, D. H.; Abdou, M. M. Oxidative stress in Egyptian children with autism: relation to autoimmunity. J Neuroimmunol 219:114-118; 2010.
53. Al-Gadani, Y.; El-Ansary, A.; Attas, O.; Al-Ayadhi, L. Metabolic biomarkers related to oxidative stress and antioxidant status in Saudi autistic children. Clin Biochem 42:1032-1040; 2009.
54. Geier, D. A.; Kern, J. K.; Garver, C. R.; Adams, J. B.; Audhya, T.; Geier, M. R. A prospective study of transsulfuration biomarkers in autistic disorders. Neurochem Res 34:386-393; 2009.
55. Krajkovicova-Kudlackova, M.; Valachovicova, M.; Mislanova, C.; Hudecova, Z.; Sudstrova, M.; Ostatnikova, D. Plasma concentration of selected antioxidants in autistic children and adolescents. Bratisl Lek Listy 110:247-250; 2009.
56. Suh, J. H.; Walsh, W. J.; McGinnis, W. R.; Lewis, A.; Ames, B. N. Altered sulfur amino acid metabolism in immune cells of children diagnosed with autism. Am J Biochem Biotechnol 4:105-113; 2008.
57. Adams, M.; Lucock, M.; Stuart, J.; Fardell, S.; Baker, K.; Ng, X. Preliminary evidence for involvement of the folate gene polymorphism 19 bp deletion-DHFR in occurrence of autism. Neurosci Lett 422:24-29; 2007.
58. Adams, J. B.; George, F.; Audhya, T. Abnormally high plasma levels of vitamin B6 in children with autism not taking supplements compared to controls not taking supplements. J Alternat Complement Med 12:59-63; 2006.
59. Adams, J. B.; Holloway, C. Pilot study of a moderate dose multivitamin/mineral supplement for children with autistic spectrum disorder. J Alternat Complement Med 10:1033-1039; 2004. (Erratum published in J. Alternat. Complement Med. 11: 749; 2005).
60. James, S. J.; Melnyk, S.; Jernigan, S.; Cleves, M. A.; Halsted, C. H.; Wong, D. H.; Cutler, P.; Bock, K.; Boris, M.; Bradstreet, J. J.; Baker, S. M.; Gaylor, D. W. Metabolic endophenotype and related genotypes are associated with oxidative stress in children with autism. Am J Med Genet B Neuropsychiatr Genet 141B:947-956; 2006.
61. Pas-ca, S. P.; Nemes, B.; Vlase, L.; Gagyi, C. E.; Dronca, E.; Miu, A. C.; Dronca, M. High levels of homocysteine and low serum paraoxonase 1 arylesterase activity in children with autism. Life Sci 78:2244-2248; 2006.
62. Tórsdóttir, G.; Hreidarsson, S.; Kristinsson, J.; Snaedal, J.; Jóhannesson, T. Ceruloplasmin, superoxide dismutase and copper in autistic patients. Basic Clin Pharmacol Toxicol 96:146-148; 2005.
63. James, S. J.; Cutler, P.; Melnyk, S.; Jernigan, S.; Janak, L.; Gaylor, D. W.; Neubrander, J. A. Metabolic biomarkers of increased oxidative stress and impaired methylation capacity in children with autism. Am J Clin Nutr 80:1611-1617; 2004.
64. Sweeten, T. L.; Posey, D. J.; Shankar, S.; McDougle, C. J. High nitric oxide production in autistic disorder: a possible role for interferon-g. Biol Psychiatry 55:434-437; 2004.
65. Zoroǧlu, S. S.; Armutcu, F.; Ozen, S.; Gurel, A.; Sivasli, E.; Yetkin, O.; Meram, I. Increased oxidative stress and altered activities of erythrocyte free radical scavenging enzymes in autism. Eur Arch Psychiatry Clin Neurosci 254:143-147; 2004.
66. Söǧüt, S.; Zoro¢glu, S. S.; Özyurt, H.; Yilmaz, H. R.; Özuǧurlu, F.; Sivasli, E.; Yetkin, O.; Yanik, M.; Tutkun, H.; Savas-, H. A.; Tarakçioǧluh, M.; Akyol, O. Changes in nitric oxide levels and antioxidant enzyme activities may have a role in the pathophysiological mechanisms involved in autism. Clin Chim Acta 331:111-117; 2003.
67. Fatemi, S. H.; Stary, J. M.; Egan, E. A. Reduced blood levels of reelin as a vulnerability factor in pathophysiology of autistic disorder. Cell Mol Neurobiol 22:139-152; 2002.
68. Yorbik, O.; Sayal, A.; Akay, C.; Akbiyik, D. I.; Sohmen, T. Investigation of antioxidant enzymes in children with autistic disorder. Prostaglandins Leukotrienes Essent Fatty Acids 67:341-343; 2002.
69. Zavala, M.; Castejó n, H. V.; Ortega, P. A.; Castejón, O. J.; Marcano de Hidalgo, A.; Montiel, N. Imbalance of plasma amino acids in patients with autism and subjects with attention deficit/hyperactivity disorder. Rev Neurol 33:401-408; 2001.
70. D'Eufemia, P.; Finocchiaro, R.; Celli, M.; Viozzi, L.; Monteleone, D.; Giardini, O. Low serum tryptophan to large neutral amino acids ratio in idiopathic infantile autism. Biomed Pharmacother 49:288-292; 1995.
71. Eto, I.; Bandy, M. D.; Butterworth Jr. C. E. Plasma and urinary levels of biopterin, neopterin, and related pterins and plasma levels of folate in infantile autism. J Autism Dev Disord 22:295-308; 1992.
72. Launay, M.; Ferrari, P.; Haimart, M.; Bursztejn, C.; Tabuteau, F.; Braconnier, A.; Pasques-Bondoux, D.; Luong, C.; Dreux, C. Serotonin metabolism and other biochemical parameters in infantile autism: a controlled study of 22 autistic children. Neuropsychobiology 20:1-11; 1988.
73. Golse, B.; Debray-Ritzen, P.; Durosay, P.; Puget, K.; Michelson, A. M. Alterations in two enzymes: superoxide dismutase and glutathione peroxidase in developmental infantile psychosis (infantile autism). Rev Neurol (Paris) 134:699-705; 1978.
74. Deeks, J. J.; Altman, D. G.; Bradburn, M. J. Statistical methods for examining heterogeneity and combining results from several studies in meta-analysis. In: Egger, M., Davey, S. G., Altman, D. G., editors. Systematic Reviews in Health Care: Meta-Analysis in Context. London: BMJ Books; 2005. p. 285-312.
75. Der Simonian, R.; Laird, N. Meta-analysis in clinical trials. Controlled Clin Trials 7:177-188; 1986.
76. Egger, M.; Davey Smith, G.; Schneider, M.; Minder, C. Bias in meta-analysis detected by a simple, graphical test. Br Med J 315:629-634; 1997.
77. Bowers, K.; Li, Q.; Bressler, J.; Avramopoulos, D.; Newschaffer, C.; Fallin, M. D. Glutathione pathway gene variation and risk of autism spectrum disorders. J Neurodev Disord 3:132-143; 2011.
78. Liu, X.; Solehdin, F.; Cohen, I. L.; Gonzalez, M. G.; Jenkins, E. C.; Lewis, M. E. S.; Holden, J. J. A. Population- and family-based studies associate the MTHFR gene with idiopathic autism in simplex families. J Autism Dev Disord 41:938-944; 2011.
79. dos Santos, P. A.; Longo, D.; Brandalize, A. P.; Schüler-Faccini, L. MTHFR C677T is not a risk factor for autism spectrum disorders in South Brazil. Psychiatr Genet 20:187-189; 2010.
80. Ming, X.; Johnson, W. G.; Stenroos, E.; Mars, A.; Lambert, G. H.; Buyske, S. Genetic variant of glutathione peroxidase 1 in autism. Brain Dev 32:105-109; 2010.
81. Mohammad, N. S.; Jain, J. M.; Chintakindi, K. P.; Singh, R. P.; Naik, U.; Akella, R. R. Aberrations in folate metabolic pathway and altered susceptibility to autism. Psychiatr Genet 19:171-176; 2009.
82. Buyske, S.; Williams, T. A.; Mars, A. E.; Stenroos, E. S.; Ming, S. X.; Wang, R.; Sreenath, M.; Factura, M. F.; Reddy, C.; Lambert, G. H.; Johnson,W. G. Analysis of case-parent trios at a locus with a deletion allele: association of GSTM1 with autism. BMC Genet 7:8; 2006.
83. Serajee, F. J.; Nabi, R.; Zhong, H.; Huq, M. Polymorphisms in xenobiotic metabolism genes and autism. J Child Neurol 19:413-417; 2004.
84. Boris, M.; Goldblatt, A.; Galanko, J.; James, S. J. Association of MTHFR gene variants with autism. J Am Physicians Surg 9:106-108; 2004.
85. Goin-Kochel, R. P.; Porter, A. E.; Peters, S. U.; Shinawi, M.; Sahoo, T.; Beaudet, A. L. The MTHFR 677C-T polymorphism and behaviors in children with autism: exploratory genotype-phenotype correlations. Autism Res 2:98-108; 2009.
86. Reed, M. C.; Thomas, R. L.; Pavisic, J.; James, S. J.; Ulrich, C. M.; Nijhout, H. F. A mathematical model of glutathione metabolism. Theor Biol Med Model 28:8; 2008.
87. Cavallaro, R. A.; Fuso, A.; Nicolia, V.; Scarpa, S. S-adenosylmethionine prevents oxidative stress and modulates glutathione metabolism in TgCRND8 mice fed a B-vitamin deficient diet. J Alzheimers Dis 20:997-1002; 2010.
88. Mosharov, E.; Cranford, M. R.; Banerjee, R. The quantitatively important relationship between homocysteine metabolism and glutathione synthesis by the transsulfuration pathway and its regulation by redox changes. Biochemistry 39:13005-13011; 2000.
89. Majumdar, S.; Mukherjee, S.; Maiti, A.; Karmakar, S.; Das, A. S.; Mukherjee, M.; Nanda, A.; Mitra, C. Folic acid or combination of folic acid and vitamin B(12) prevents short-term arsenic trioxide-induced systemic and mitochondrial dysfunction and DNA damage. Environ Toxicol 24:377-387; 2009.
90. Bagnyukova, T. V.; Powell, C. L.; Pavliv, O.; Tryndyak, V. P.; Pogribny, I. P. Induction of oxidative stress and DNA damage in rat brain by a folate/methyl-deficient diet. Brain Res 1237:44-51; 2008.
91. Melnyk, S.; Jernigan, S.; Savenka, S.; James, S. J. Elevation in S-adenosylhomocysteine and DNA hypomethylation in parents and children with autism. FASEB J 21:A348; 2007.
92. James, S. J.; Melnyk, S.; Fuchs, G.; Reid, T.; Jernigan, S.; Pavliv, O.; Hubanks; Gaylor, D. W. Efficacy of methylcobalamin and folinic acid treatment on glutathione redox status in children with autism. Am J Clin Nutr 89:425-430; 2009.
93. Lepage, N.; McDonald, N.; Dallaire, L.; Lambert, M. Age-specific distribution of plasma amino acid concentrations in a healthy pediatric population. Clin Chem 43:2397-2402; 1997.
94. Cengiz, M.; Yüksel, A.; Seven, M. The effects of carbamazepine and valproic acid on the erythrocyte glutathione, glutathione peroxidase, superoxide dismutase and serum lipid peroxidation in epileptic children. Pharmacol Res 41:423-425; 2000.
95. Yüksel, A.; Cengiz, M.; Seven, M.; Ulutin, T. Erythrocyte glutathione, glutathione peroxidase, superoxide dismutase and serum lipid peroxidation in epileptic children with valproate and carbamazepine. J Basic Clin Physiol Pharmacol 11:73-81; 2000.
96. Sobaniec, W.; Solowiej, E.; Kulak, W.; Bockowski, L.; Smigielska-Kuzia, J.; Artemowicz, B. Evaluation of the influence of antiepileptic therapy on antioxidant enzyme activity and lipid peroxidation in erythrocytes of children with epilepsy. J Child Neurol 2:558-562; 2006.
97. Varoglu, A. O.; Yildirim, A.; Aygul, R.; Gundogdu, O. L.; Sahin, Y. N. Effects of valproate, carbamazepine, and levetiracetam on the antioxidant and oxidant systems in epileptic patients and their clinical importance. Clin Neuropharmacol 33:155-157; 2010.
98. Ioannidis, J. P.; Trikalinos, T. A. The appropriateness of asymmetry tests for publication bias in meta-analyses: a large survey. Can Med Assoc J 176:1091-1096; 2007.
99. Praticò, D. Alzheimer's disease and oxygen radicals: new insights. Biochem Pharmacol 63:563-567; 2002.
100. Domenici, E.; Muglia, P.; Merlo-Pich, E. Hunting for peripheral biomarkers to support drug development in psychiatry. In: Turck, C. W., editor. Biomarkers for Psychiatric Disorders. New York: Springer Science; 2008. p. 1-22.
101. Bonatto, F.; Polydoro, M.; Andrades, M. E.; da Frota Junior, M. L.; Dal-Pizzol, F.; Rotta, L. N.; Souza, D. O.; Perry, M. L.; Moreira, J. C. Effect of protein malnutrition on redox state of the hippocampus of rat. Brain Res 1042:17-22; 2005.
102. Bederova, A.; Kudlackova, M.; Simoncinc, R.; Grancicova, E.; Magalova, T.; Brtkova, A. Total antioxidant status and antioxidative vitamins in selected group of children and adolescents. Hygienia 42:92-98; 1997.
103. Krajcovicova-Kudlackova, M.; Simoncinc, R.; Bederova, A.; Grancicova, E.; Magalova, T. Influence of vegetarian and mixed diet on selected haematological and biochemical parameters in children. Nahrung 41:311-314; 1997.