BDNF content and catalase activity in the blood of children with autism spectrum disorders

Abstract

BACKGROUND: With the increasing prevalence of autism spectrum disorders worldwide, it is relevant to study the mechanisms contributing to their development and progression. The participation of brain-derived neurotrophic factor and oxidative stress in the pathogenesis of the disease is considered, however, their role in this process remains unclear. The relationship between BDNF levels and oxidative stress in the blood of patients with autism spectrum disorders has not been studied.

AIM: The aim was to evaluate the content of brain neurotrophic factor, BDNF, and catalase, an antioxidant defense enzyme, in children with various clinical forms of autism spectrum disorders.

MATERIALS AND METHODS: BDNF content and catalase activity were assessed in the blood plasma of 78 children with autism spectrum disorders, including 41 patients with childhood autism, 19 children with atypical autism, 6 patients with Asperger’s syndrome, and 12 patients with other general developmental disorders (with elements of autism). The control group consisted of 20 conditionally healthy children. The diagnosis was established in accordance with the ICD-10. The severity of disorders was determined using the Childhood Autism Rating Scale. The content of BDNF was evaluated using the method of enzyme immunoassay, catalase activity was determined by colorimetric method.

RESULTS: The content of BDNF in blood plasma was reduced in children with autism spectrum disorders compared to its levels in control group subjects. BDNF levels depended on the clinical form of the disease: the content of BDNF was reduced in patients with childhood autism, atypical autism, Asperger’s syndrome compared to control group subjects; in patients with atypical autism it is lower than in patients with childhood autism; BDNF levels in the group of patients with other general developmental disorders and in control group did not differ. The content of BDNF did not depend on gender, age and severity of autism spectrum disorders. A negative correlation was found between BDNF levels and the age of control group children. There were no differences in the activity of catalase in the blood of children with autism spectrum disorders and in control group. A positive correlation was found between BDNF levels and catalase activity in children with autism spectrum disorders and control group subjects.

CONCLUSIONS: A decrease in the content of BDNF in the blood of children with autism spectrum disorders was revealed. Neurotrophin content differed in children with separate clinical forms of the disease. To varying degrees the decrease in BDNF levels in patients with childhood autism, atypical autism, Asperger’s syndrome and the absence of changes in patients with other general developmental disorders compared with controls could be associated with a different contribution of neurotrophin to the pathogenesis of clinical forms of autism spectrum disorders. In children with autism spectrum disorders, there were no age-related changes in neurotrophin levels, while in healthy children a negative correlation was found between the content of BDNF and age. The absence of changes in the activity of catalase in the blood of children with autism spectrum disorders indicated the safety of the antioxidant defense system in terms of this indicator. The positive correlation between BDNF levels and catalase activity in the blood of patients with autism spectrum disorders and control group subjects reflected the protective role of neurotrophin from the damaging effects of oxidative stress.

Keywords

autism spectrum disorders / BDNF / oxidative stress / catalase

References

[1] American Psychiatric Association, DSM-5 Task Force. Diagnostic and statistical manual of mental disorders. 5th ed. American Psychiatric Publishing, Inc. 2013. DOI: 10.1176/appi.books.9780890425596

[2] American Psychiatric Association, DSM-5 Task Force. Diagnostic and statistical manual of mental disorders. 5th ed. American Psychiatric Publishing, Inc, 2013. DOI: 10.1176/appi.books.9780890425596

[3] International Statistical Classification of Diseases and Related Health Problems; 10th revision: Updates 1998–2012. http://www. who.int/classifications/icd/icd10updates/en/index.html.

[4] Essa MM, Qoronfleh MW., eds. Personalized Food Intervention and Therapy for Autism Spectrum Disorder Management. Advances in Neurobiology. 2020. Vol. 24. DOI: 10.1007/978-3-030-30402-7

[5] Personalized Food Intervention and Therapy for Autism Spectrum Disorder Management. Ed. by M.M. Essa, M.W. Qoronfleh // Advances in Neurobiology. 2020. Vol. 24. DOI: 10.1007/978-3-030-30402-7

[6] Belokoskova SG, Malsagova EM, Tsikunov SG. Dynamics of age-related structural and functional changes in the brain of patients with autism spectrum disorders. Medical Academic Journal. 2019:19(3);21–26. (In Russ.) DOI: 10.17816/MAJ19321-26

[7] Белокоскова С.Г., Мальсагова Э.М., Цикунов С.Г. Динамика возрастных структурно-функциональных изменений мозга больных расстройствами аутистического спектра // Медицинский академический журнал. 2019. Т. 19, № 3. С. 21–26. DOI: 10.17816/MAJ19321-26

[8] Сourchesne E, Pramparo T, Gazestani VH, et al. The ASD Living Biology: from cell proliferation to clinical phenotype. Mol Psychiatry. 2019;24(1):88–107. DOI: 10.1038/s41380-018-0056-y

[9] Сourchesne E., Pramparo T., Gazestani V.H. et al. The ASD Living Biology: from cell proliferation to clinical phenotype // Mol. Psychiatry. 2019. Vol. 24, No. 1. P. 88–107. DOI: 10.1038/s41380-018-0056-y

[10] Chapleau CA, Larimore JL, Theibert A, Pozzo-Miller L. Modulation of dendritic spine development and plasticity by BDNF and vesicular trafficking: fundamental roles in neurodevelopmental disorders associated with mental retardation and autism. J Neurodev Disord. 2009;1(3):185–196. DOI: 10.1007/s11689-009-9027-6

[11] Chapleau C.A., Larimore J.L., Theibert A., Pozzo-Miller L. Modulation of dendritic spine development and plasticity by BDNF and vesicular trafficking: fundamental roles in neurodevelopmental disorders associated with mental retardation and autism // J. Neurodev. Disord. 2009. Vol. 1, No. 3. P. 185–196. DOI: 10.1007/s11689-009-9027-6

[12] Turovskaya MV, Gaidin SG, Vedunova MV, et al. BDNF overexpression enhances the preconditioning effect of brief episodes of hypoxia, promoting survival of GABAergic neurons. Neurosci Bull. 2020;36(7):733–760. DOI: 10.1007/s12264-020-00480-z

[13] Turovskaya M.V., Gaidin S.G., Vedunova M.V. et al. BDNF overexpression enhances the preconditioning effect of brief episodes of hypoxia, promoting survival of GABAergic neurons // Neurosci. Bull. 2020. Vol. 36, No. 7. P. 733–760. DOI: 10.1007/s12264-020-00480-z

[14] Miyazaki K, Narita N, Sakuta R, et al. Serum neurotrophin concentrations in autism and mental retardation: a pilot study. Brain Dev. 2004;26(5):292–295. DOI: 10.1016/S0387-7604(03)00168-2

[15] Miyazaki K., Narita N., Sakuta R. et al. Serum neurotrophin concentrations in autism and mental retardation: a pilot study // Brain Dev. 2004. Vol. 26, No. 5. P. 292–295. DOI: 10.1016/S0387-7604(03)00168-2

[16] Connolly AM, Chez M, Streif EM, et al. Brain-derived neurotrophic factor and autoantibodies to neural antigens in sera of children with autistic spectrum disorders, Landau–Kleffner syndrome, and epilepsy. Biol Psychiatry. 2006;59(4):354–363. DOI: 10.1016/j.biopsych.2005.07.004

[17] Connolly A.M., Chez M., Streif E.M. et al. Brain-derived neurotrophic factor and autoantibodies to neural antigens in sera of children with autistic spectrum disorders, Landau–Kleffner syndrome, and epilepsy // Biol. Psychiatry. 2006. Vol. 59, No. 4. P. 354–363. DOI: 10.1016/j.biopsych.2005.07.004

[18] Katoh-Semba R, Wakako R, Komori T, et al. Age-related changes in BDNF protein levels in human serum: Differences between autism cases and normal controls. Int J Dev Neurosci. 2007;25(6):367–372. DOI: 10.1016/j.ijdevneu.2007.07.002

[19] Katoh-Semba R., Wakako R., Komori T. et al. Age-related changes in BDNF protein levels in human serum: Differences between autism cases and normal controls // Int. J. Dev. Neurosci. 2007. Vol. 25, No. 6. P. 367–372. DOI: 10.1016/j.ijdevneu.2007.07.002

[20] Correia CT, Coutinho AM, Sequeira AF, et al. Increased BDNF levels and NTRK2 gene association suggest a disruption of BDNF/TrkB signaling in autism. Genes Brain Behav. 2010;9(7):841–848. DOI: 10.1111/j.1601-183X.2010.00627.x

[21] Correia C.T., Coutinho A.M., Sequeira A.F. et al. Increased BDNF levels and NTRK2 gene association suggest a disruption of BDNF/TrkB signaling in autism // Genes Brain Behav. 2010. Vol. 9, No. 7. P. 841–848. DOI: 10.1111/j.1601-183X.2010.00627.x

[22] Taurines R, Segura M, Schecklmann M, et al. Altered peripheral BDNF mRNA expression and BDNF protein concentrations in blood of children and adolescents with autism spectrum disorder. J Neural Transm (Vienna). 2014;121(9):1117–1128. DOI: 10.1007/s00702-014-1162-x

[23] Taurines R., Segura M., Schecklmann M. et al. Altered peripheral BDNF mRNA expression and BDNF protein concentrations in blood of children and adolescents with autism spectrum disorder // J. Neural. Transm. (Vienna). 2014. Vol. 121, No. 9. P. 1117–1128. DOI: 10.1007/s00702-014-1162-x

[24] Bryn V, Halvorsen B, Ueland T, et al. Brain derived neurotrophic factor (BDNF) and autism spectrum disorders (ASD) in childhood. Eur J Paediatr Neurol. 2015;19(4):411–414. DOI: 10.1016/j.ejpn.2015.03.005

[25] Bryn V., Halvorsen B., Ueland T. et al. Brain derived neurotrophic factor (BDNF) and autism spectrum disorders (ASD) in childhood // Eur. J. Paediatr. Neurol. 2015. Vol. 19, No. 4. P. 411–414. DOI: 10.1016/j.ejpn.2015.03.005

[26] Francis K, Dougali A, Sideri K, et al. Brain-derived neurotrophic factor (BDNF) in children with ASD and their parents: a 3-year follow-up. Acta Psychiatr Scand. 2018;137(5):433–441. DOI: 10.1111/acps.12872

[27] Francis K., Dougali A., Sideri K. et al. Brain-derived neurotrophic factor (BDNF) in children with ASD and their parents: a 3-year follow-up // Acta Psychiatr. Scand. 2018. Vol. 137, No. 5. P. 433–441. DOI: 10.1111/acps.12872

[28] Bjørklund G, Meguid NA, El-Ansary A. Diagnostic and severity-tracking biomarkers for autism spectrum disorder. J Mol Neurosci. 2018;66(4):492–511. DOI: 10.1007/s12031-018-1192-1191

[29] Bjørklund G., Meguid N.A., El-Ansary A. Diagnostic and severity-tracking biomarkers for autism spectrum disorder // J. Mol. Neurosci. 2018. Vol. 66, No. 4. P. 492–511. DOI: 10.1007/s12031-018-1192-1191

[30] Zoroglu SS, Armutcu F, Ozen S, et al. Increased oxidative stress and altered activities of erythrocyte free radical scavenging enzymes in autism. Eur Arch Psychiatry Clin Neurosci. 2004;254(3):143–147. DOI: 10.1007/s00406-004-0456-7

[31] Zoroglu S.S., Armutcu F., Ozen S. et al. Increased oxidative stress and altered activities of erythrocyte free radical scavenging enzymes in autism // Eur. Arch. Psychiatry Clin. Neurosci. 2004. Vol. 254, No. 3. P. 143–147. DOI: 10.1007/s00406-004-0456-7

[32] Kondolot M, Ozmert EN, Ascı A, et al. Plasma phthalate and bisphenol a levels and oxidant-antioxidant status in autistic children. Environ Toxicol Pharmacol. 2016;43:149–158. DOI: 10.1016/j.etap.2016.03.006

[33] Kondolot M., Ozmert E.N., Ascı A. et al. Plasma phthalate and bisphenol a levels and oxidant-antioxidant status in autistic children // Environ. Toxicol. Pharmacol. 2016. Vol. 43. P. 149–158. DOI: 10.1016/j.etap.2016.03.006

[34] Yenkoyan K, Harutyunyan H, Harutyunyan A. A certain role of SOD/CAT imbalance in pathogenesis of autism spectrum disorders. Free Radic Biol Med. 2018;123:85–95. DOI: 10.1016/j.freeradbiomed.2018.05.070

[35] Yenkoyan K., Harutyunyan H., Harutyunyan A. A certain role of SOD/CAT imbalance in pathogenesis of autism spectrum disorders // Free Radic. Biol. Med. 2018. Vol. 123. P. 85–95. DOI: 10.1016/j.freeradbiomed.2018.05.070

[36] Al-Ayadhi LY. Relationship between Sonic hedgehog protein, brain-derived neurotrophic factor and oxidative stress in autism spectrum disorders. Neurochem Res. 2012;37(2):394–400. DOI: 10.1007/s11064-011-0624-x

[37] Al-Ayadhi L.Y. Relationship between Sonic hedgehog protein, brain-derived neurotrophic factor and oxidative stress in autism spectrum disorders // Neurochem. Res. 2012. Vol. 37, No. 2. P. 394–400. DOI: 10.1007/s11064-011-0624-x

[38] Lord C, Rutter M, Le Couteur A. Autism diagnostic interview-revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. J Autism Dev Disord. 1994;24(5):659–685. DOI: 10.1007/BF02172145

[39] Lord C., Rutter M., Le Couteur A. Autism diagnostic interview-revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders // J. Autism. Dev. Disord. 1994. Vol. 24, No. 5. P. 659–685. DOI: 10.1007/BF02172145

[40] Schopler E, Reichler RJ, DeVellis RF, Daly K. Toward objective classifcation of childhood autism: Childhood Autism Rating Scale (CARS). J Autism Dev Disord. 1980;10(1):91–103. DOI: 10.1007/BF02408436

[41] Schopler E., Reichler R.J., DeVellis R.F., Daly K. Toward objective classifcation of childhood autism: Childhood Autism Rating Scale (CARS) // J. Autism. Dev. Disord. 1980. Vol. 10, No. 1. P. 91–103. DOI: 10.1007/BF02408436

[42] Sharma SR, Gonda X, Tarazi FI. Autism spectrum disorder: Classification, diagnosis and therapy. Pharmacol Ther. 2018;190:91–104. DOI: 10.1016/j.pharmthera.2018.05.007

[43] Sharma S.R., Gonda X., Tarazi F.I. Autism spectrum disorder: Classification, diagnosis and therapy // Pharmacol. Ther. 2018. Vol. 190. P. 91–104. DOI: 10.1016/j.pharmthera.2018.05.007

[44] Zheng Z, Zhang L, Zhu T, et al. Peripheral brain-derived neurotrophic factor in autism spectrum disorder: a systematic review and meta-analysis. Sci Rep. 2016;6:31241. DOI: 10.1038/srep31241

[45] Zheng Z., Zhang L., Zhu T. et al. Peripheral brain-derived neurotrophic factor in autism spectrum disorder: a systematic review and meta-analysis // Sci. Rep. 2016. Vol. 6. P. 31241. DOI: 10.1038/srep31241

[46] Saghazadeh A, Rezaei N. Brain-derived neurotrophic factor levels in autism: a systematic review and meta-analysis. J Autism Dev Disord. 2017;47(4):1018–1029. DOI: 10.1007/s10803-016-3024-x

[47] Saghazadeh A., Rezaei N. Brain-derived neurotrophic factor levels in autism: a systematic review and meta-analysis // J. Autism. Dev. Disord. 2017. Vol. 47, No. 4. P. 1018–1029. DOI: 10.1007/s10803-016-3024-x

[48] Mattson MP, Duan W, Guo Z. Meal size and frequency affect neuronal plasticity and vulnerability to disease: cellular and molecular mechanisms. J Neurochem. 2003;84(3):417–431. DOI: 10.1046/j.1471-4159.2003.01586.x

[49] Mattson M.P., Duan W., Guo Z. Meal size and frequency affect neuronal plasticity and vulnerability to disease: cellular and molecular mechanisms // J. Neurochem. 2003. Vol. 84, No. 3. P. 417–431. DOI: 10.1046/j.1471-4159.2003.01586.x

[50] Skogstrand K, Hagen CM, Borbye-Lorenzen N, et al. Reduced neonatal brain-derived neurotrophic factor is associated with autism spectrum disorders. Transl Psychiatry. 2019;9(1):252. DOI: 10.1038/s41398-019-0587-2

[51] Skogstrand K., Hagen C.M., Borbye-Lorenzen N. et al. Reduced neonatal brain-derived neurotrophic factor is associated with autism spectrum disorders // Transl. Psychiatry. 2019. Vol. 9, No. 1. P. 252. DOI: 10.1038/s41398-019-0587-2

[52] Tapia-Arancibia L, Rage F, Givalois L, Arancibia S. Physiology of BDNF: focus on hypothalamic function. Front Neuroendocrinol. 2004;25(2):77–107. DOI: 10.1016/j.yfrne.2004.04.001

[53] Tapia-Arancibia L., Rage F., Givalois L., Arancibia S. Physiology of BDNF: focus on hypothalamic function // Front. Neuroendocrinol. 2004. Vol. 25, No. 2. P. 77–107. DOI: 10.1016/j.yfrne.2004.04.001

[54] Yoshida T, Ishikawa M, Niitsu T, et al. Decreased serum levels of mature brain-derived neurotrophic factor (BDNF), but not its precursor proBDNF, in patients with major depressive disorder. PLoS One. 2012;7(8):e42676. DOI: 10.1371/journal.pone.0042676

[55] Yoshida T., Ishikawa M., Niitsu T. et al. Decreased serum levels of mature brain-derived neurotrophic factor (BDNF), but not its precursor proBDNF, in patients with major depressive disorder // PLoS One. 2012. Vol. 7, No. 8. P. e42676. DOI: 10.1371/journal.pone.0042676

[56] Ng TKS, Ho CSH, Tam WWS, et al. Decreased serum brain-derived neurotrophic factor (BDNF) levels in patients with Alzheimer’s disease (AD): A systematic review and meta-analysis. Int J Mol Sci. 2019;20(2):257. DOI: 10.3390/ijms20020257

[57] Ng T.K.S., Ho C.S.H., Tam W.W.S. et al. Decreased serum brain-derived neurotrophic factor (BDNF) levels in patients with Alzheimer’s disease (AD): A systematic review and meta-analysis // Int. J. Mol. Sci. 2019. Vol. 20, No. 2. P. 257. DOI: 10.3390/ijms20020257

[58] Singh J, Verma R, Raghav R, et al. Brain-derived neurotrophic factor (BDNF) levels in first-episode schizophrenia and healthy controls: A comparative study. Asian J Psychiatr. 2020;54:102370. DOI: 10.1016/j.ajp.2020.102370

[59] Singh J., Verma R., Raghav R. et al. Brain-derived neurotrophic factor (BDNF) levels in first-episode schizophrenia and healthy controls: A comparative study // Asian J. Psychiatr. 2020. Vol. 54. P. 102370. DOI: 10.1016/j.ajp.2020.102370

[60] Numakawa T, Odaka H, Adachi N. Actions of brain-derived neurotrophin factor in the neurogenesis and neuronal function, and its involvement in the pathophysiology of brain diseases. Int J Mol Sci. 2018;19(11):3650. DOI: 10.3390/ijms19113650

[61] Numakawa T., Odaka H., Adachi N. Actions of brain-derived neurotrophin factor in the neurogenesis and neuronal function, and its involvement in the pathophysiology of brain diseases // Int. J. Mol. Sci. 2018. Vol. 19, No. 11. P. 3650. DOI: 10.3390/ijms19113650

[62] Chomiak T, Hu B. Alterations of neocortical development and maturation in autism: insight from valproic acid exposure and animal models of autism. Neurotoxicol Teratol. 2013;36:57–66. DOI: 10.1016/j.ntt.2012.08.005

[63] Chomiak T., Hu B. Alterations of neocortical development and maturation in autism: insight from valproic acid exposure and animal models of autism // Neurotoxicol. Teratol. 2013. Vol. 36. P. 57–66. DOI: 10.1016/j.ntt.2012.08.005

[64] Meng WD, Sun SJ, Yang J, et al. Elevated serum brain-derived neurotrophic factor (BDNF) but not BDNF Gene Val66Met polymorphism is associated with autism spectrum disorders. Mol Neurobiol. 2017;54(2):1167–1172. DOI: 10.1007/s12035-016-9721-9

[65] Meng W.D., Sun S.J., Yang J. et al. Elevated serum brain-derived neurotrophic factor (BDNF) but not BDNF Gene Val66Met polymorphism is associated with autism spectrum disorders // Mol. Neurobiol. 2017. Vol. 54, No. 2. P. 1167–1172. DOI: 10.1007/s12035-016-9721-9

[66] Belokoskova SG, Tsikunov SG. Antioxidant and prooxidant systems in patients with ischemic insult. Reviews on Clinical Pharmacology and Drug Therapy. 2021;19(3):281–290. (In Russ.) DOI: 10.17816/RCF193281-290

[67] Белокоскова С.Г., Цикунов С.Г. Антиоксидантная и прооксидантная система у больных ишемическим инсультом // Обзоры по клинической фармакологии и лекарственной терапии. 2021. Т. 19, № 3. С. 281–290. DOI: 10.17816/RCF193281-290

[68] Mattson MP, Lovell MA, Furukawa K, et al. Neurotrophic factors attenuate glutamate-induced accumulation of peroxides, elevation of intracellular Ca2+ concentration, and neurotoxicity and increase antioxidant enzyme activities in hippocampal neurons. J Neurochem. 1995;65:1740–1751. DOI: 10.1046/j.1471-4159.1995.65041740.x

[69] Mattson M.P., Lovell M.A., Furukawa K. et al. Neurotrophic factors attenuate glutamate-induced accumulation of peroxides, elevation of intracellular Ca2+ concentration, and neurotoxicity and increase antioxidant enzyme activities in hippocampal neurons // J. Neurochem. 1995. Vol. 65. P. 1740–1751. DOI: 10.1046/j.1471-4159.1995.65041740.x

[70] Valvassori SS, Arent CO, Steckert AV, et al. Intracerebral administration of BDNF protects rat brain against oxidative stress induced by ouabain in an animal model of mania. Mol Neurobiol. 2015;52(1):353–362. DOI: 10.1007/s12035-014-8873-8

[71] Valvassori S.S., Arent C.O., Steckert A.V. et al. Intracerebral administration of BDNF protects rat brain against oxidative stress induced by ouabain in an animal model of mania // Mol. Neurobiol. 2015. Vol. 52, No. 1. P. 353–362. DOI: 10.1007/s12035-014-8873-8

[72] Poduslo JF, Curran GL. Permeability at the blood-brain and blood-nerve barriers of the neurotrophic factors: NGF, CNTF, NT-3, BDNF. Brain Res Mol Brain Res. 1996;36(2):280–286. DOI: 10.1016/0169-328x(95)00250-v

[73] Poduslo J.F., Curran G.L. Permeability at the blood-brain and blood-nerve barriers of the neurotrophic factors: NGF, CNTF, NT-3, BDNF // Brain Res. Mol. Brain Res. 1996. Vol. 36, No. 2. P. 280–286. DOI: 10.1016/0169-328x(95)00250-v

[74] Pan W, Banks WA, Fasold MB, et al. Transport of brain-derived neurotrophic factor across the blood-brain barrier. Neuropharmacology. 1998;37(12):1553–1561. DOI: 10.1016/s0028-3908(98)00141-5

[75] Pan W., Banks W.A., Fasold M.B. et al. Transport of brain-derived neurotrophic factor across the blood-brain barrier // Neuropharmacology. 1998. Vol. 37, No. 12. P. 1553–1561. DOI: 10.1016/s0028-3908(98)00141-5.

[76] Zoladz JA, Pilc A, Majerczak J, et al. Endurance training increases plasma brain-derived neurotrophic factor concentration in young healthy men. J Physiol Pharmacol. 2008;59 Suppl 7:119–132.

[77] Zoladz J.A., Pilc A., Majerczak J. et al. Endurance training increases plasma brain-derived neurotrophic factor concentration in young healthy men // J. Physiol. Pharmacol. 2008. Vol. 59 Suppl 7. P. 119–132.

[78] Sánchez-Villegas A, Galbete C, Martinez-González MA, et al. The effect of the Mediterranean diet on plasma brain-derived neurotrophic factor (BDNF) levels: the PREDIMED-NAVARRA randomized trial. Nutr Neurosci. 2011;14(5):195–201. DOI: 10.1179/1476830511Y.0000000011

[79] Sánchez-Villegas A., Galbete C., Martinez-González M.A. et al. The effect of the Mediterranean diet on plasma brain-derived neurotrophic factor (BDNF) levels: the PREDIMED-NAVARRA randomized trial // Nutr. Neurosci. 2011. Vol. 14, No. 5. P. 195–201. DOI: 10.1179/1476830511Y.0000000011

[80] Matsuoka Y, Nishi D, Tanima Y, et al. Serum pro-BDNF/BDNF as a treatment biomarker for response to docosahexaenoic acid in traumatized people vulnerable to developing psychological distress: a randomized controlled trial. Transl Psychiatry. 2015;5(7):e596. DOI: 10.1038/tp.2015.89

[81] Matsuoka Y., Nishi D., Tanima Y. et al. Serum pro-BDNF/BDNF as a treatment biomarker for response to docosahexaenoic acid in traumatized people vulnerable to developing psychological distress: a randomized controlled trial // Transl. Psychiatry. 2015. Vol. 5, No. 7. P. e596. DOI: 10.1038/tp.2015.89

[82] Glud M, Christiansen T, Larsen LH, et al. Changes in circulating BDNF in relation to sex, diet, and exercise: A 12-week randomized controlled study in overweight and obese participants. J Obes. 2019;2019:4537274. DOI: 10.1155/2019/4537274

[83] Glud M., Christiansen T., Larsen L.H. et al. Changes in circulating BDNF in relation to sex, diet, and exercise: A 12-week randomized controlled study in overweight and obese participants // J. Obes. 2019. Vol. 2019. P. 4537274. DOI: 10.1155/2019/4537274

[84] Anokhin PK, Veretinskaya AG, Pavshintsev VV, Shamakina IYu. The effect of the dopamine D2 receptor agonist cabergoline on the content of catecholamines and expression of BDNF mRNA in the rat midbrain and hypothalamus. S.S. Korsakov Journal of Neurology and Psychiatry. 2019;119(11):54–59. (In Russ.) DOI: 10.17116/jnevro201911911154

[85] Анохин П.К., Веретинская А.Г., Павшинцев В.В., Шамакина И.Ю. Влияние агониста дофаминовых D2-рецепторов каберголина на содержание катехоламинов и экспрессию мРНК BDNF в среднем мозге и гипоталамусе в эксперименте // Журнал неврологии и психиатрии им. С.С. Корсакова. 2019. Т. 119, № 11. С. 54–59. DOI: 10.17116/jnevro201911911154

[86] Belokoskova SG, Kritskaya DV, Beznin GV, et al. 1-Desamino-8-D-arginin-vasopressin, DDAVP, increases the content of brain-derived neurotrophic factor (BDNF) in blood plasma of rats in model of post-traumatic stress disorders. Medical Academic Journal. 2020;20(4):27–34. (In Russ.) DOI: 10.17816/MAJ46393

[87] Белокоскова С.Г., Крицкая Д.В., Безнин Г.В. и др. 1-Дезамино-8-D-аргинин-вазопрессин увеличивает содержание нейротрофического фактора мозга (BDNF) в плазме крови у крыс в модели посттравматического стрессового расстройства // Медицинский академический журнал. 2020. Т. 20, № 4. С. 27–34. DOI: 10.17816/MAJ46393

RIGHTS & PERMISSIONS

Eco-Vector