Biomarkers of oxidative stress and proteopathies in the diagnosis of neurodegenerative diseases

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Abstract

Introduction. Despite numerous studies in the field of neurodegenerative diseases, the exact mechanisms of these processes have not yet been identified.

The purpose of this review is to analyze the methodological approaches necessary to revise the traditional and create new reliable prognostic and diagnostic algorithms that reflect pathogenetic features at different stages of neurodegeneration and atypical course of the disease.

Material and methods. The review highlights the results of clinical and experimental studies obtained using a complex of clinical, laboratory and instrumental methods with an emphasis on markers of oxidative stress and proteopathy. In preparing the materials, sources from international and domestic databases were used: Scopus, Web of Science, Pub Medline, RSCI mainly for the last 15 years.

Results. An idea has been formed about the molecular mechanisms of neural tissue regression in a number of neurodegenerative diseases such as multiple sclerosis, amyotrophic lateral sclerosis, Alzheimer’s and Parkinson’s disease. The relationship between the parameters of the oxidative process and the features of metal-energy shifts in organs and organ systems is demonstrated. The role of markers of oxidative stress in the early stages, when the process of inflammation prevails and in the atypical course of the disease, is shown. Valuable biochemical markers are cytokines, glutathione levels, myeloperoxidase activation, and isoprostanes. The review points to the prospect of including in screening indicators of iron and other metals such as Zn, Mg, affecting the clinic accumulation of β-amyloid, in connection with which they can be considered as the basis for the progression of neurodegeneration. New data on the contribution of halogenating stress to the pathogenesis of neuroinflammation are presented. An aspect requiring development in the field of biomarkers for assessing the duration of the disease and prognostic prospects is the data on the correlation of metabolic shifts in the intestinal microbiota with the duration of the disease and the inflammatory process. Essential for the creation of express diagnostic methods is the determination of redox balance as an integral marker in saliva, which has obvious advantages over the use of biological fluids, such as liquor and serum.

Conclusion. The prospects of creating new prognostic and diagnostic schemes are associated with complexes, including laboratory and instrumental methods, in blood, liquor and saliva. Evaluation of the sensitivity and specificity of new markers depending on the clinical diagnosis allows the selection of pathogenetically significant markers in the early stages of the disease, with atypical neurodegeneration, to establish subtypes of the disease, to carry out their differential diagnosis.

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About the authors

Zoya I. Mikashinovich

Federal State Budgetary Educational Institution of Higher Professional Education «Rostov State Medical University» Ministry of Health of the Russian Federation

Author for correspondence.
Email: mikashinovich@gmail.com
ORCID iD: 0000-0001-9906-8248

Doctor of Biological Sciences, Professor, Professor of the Department of General and Clinical Biochemistry No. 1

Russian Federation, Nakhichevansky per. 29, Rostov-on-Don, 344022

Natalia R. Telesmanich

Federal State Budgetary Educational Institution of Higher Professional Education «Rostov State Medical University» Ministry of Health of the Russian Federation

Email: telesmanich.nr@gmail.com
ORCID iD: 0000-0002-1906-6312

Doctor of Biological Sciences, Professor, Professor of the Department of General and Clinical Biochemistry No. 1 

Russian Federation, Nakhichevansky per. 29, Rostov-on-Don, 344022

Olga B. Smirnova

Federal State Budgetary Educational Institution of Higher Professional Education «Rostov State Medical University» Ministry of Health of the Russian Federation

Email: zolochevskaj51@mail.ru
ORCID iD: 0000-0003-4402-2474

Candidate of Biological Sciences, Senior Lecturer of the Department of General and Clinical Biochemistry No.1

Russian Federation, Nakhichevansky per. 29, Rostov-on-Don, 344022

Elena A. Chernogubova

Federal State Budgetary Institution of Science «Federal Research Center Southern Scientific Center of the Russian Academy of Sciences» of the Ministry of Science and Higher Education of the Russian Federation

Email: eachernogubova@mail.ru
ORCID iD: 0000-0001-5128-4910

Ph.D. Leading Researcher, Head Laboratory of Experimental Biology

Russian Federation, 344006, Rostov-on-Don, Chekhov Ave., 41

References

  1. Тапахов А.А., Попова Т.Е., Николаева Т.Я., Шнайдер Н.А., Петрова М.М. Эпидемиология болезни Паркинсона в мире и в России. Забайкальский медицинский вестник. 2016; 4: 151–9. [Tapahov A.A., Popova T.E., Nikolaeva T.YA. Shnajder N.A., Petrova M.M. Epidemiology of parkinson’s disease in the world and Russia. Zabajkal’skij medicinskij vestnik. 2016; 4: 151–9 (in Russian)].
  2. Раздорская В.В., Воскресенская О.Н., Юдина Г.К. Болезнь Паркинсона в России: распространенность и заболеваемость (обзор). Саратовский научно-медицинский журнал. 2016; 12 (3): 379–84. [Razdorskaya V.V., Voskresenskaya O.N., Yudina G.K. Parkinson’s disease in Russia: prevalence and incidence (review). Saratovskij nauchno-medicinskij zhurnal. 2016; 12 (3): 379–84 (in Russian)].
  3. Piazza J.R., Almeida D.M., Dmitrieva N.O., Klein L.C. Frontiers in the use of biomarkers of health in research on stress and aging. J. Gerontology: Psychological Sciences. 2010; 65 (5): 513–25. doi: 10.1093/geronb/gbq049
  4. Gao J., Wang L., Liu J., Xie F., Su B., Wang X. Abnormalities of Mitochondrial Dynamics in Neurodegenerative Diseases. Antioxidants (Basel). 2017; 6 (2): 25. doi: 10.3390/antiox6020025
  5. Гапонов Д.О., Пригодина Е.В., Грудина Т.В. Современный взгляд на патогенетические механизмы прогрессирования болезни Паркинсона. РМЖ. 2018; 26 (12–1): 66–72. [Gaponov D.O., Prigodina E.V., Grudina T.V. Modern view on the pathogenetic mechanisms of Parkinson’s disease progression. RMZH. 2018; 26 (12–1): 66–72 (in Russian)].
  6. Гончарова 3.A., Колмакова Т.С, Оксенюк О.С. Моргуль Е.В., Гельпей М.А., Калмыкова Ю.А., Смирнова О.Б., Муталиева Х.М. Мультипараметрическая оценка биохимических маркеров крови при болезни Паркинсона. Практическая медицина. 2018; 10: 87–91. doi: 10.32000/2072-1757-2018-10-87-91 [Goncharova 3.A., Kolmakova T. S, Oksenyuk O. S. Morgul’ E.V., Gel’pej M. A., Kalmykova YU.A., Smirnova O. B., Mutalieva Kh. M. Multi-parametric assessment of biochemical blood markers in Parkinson’s disease. Prakticheskaya medicina. 2018; 10: 87–91. doi: 10.32000/2072-1757-2018-10-87-91] (in Russian)].
  7. Левин О.С., Боголепова А.Н. Когнитивная реабилитация пациентов с нейродегенеративными заболеваниями. Журнал неврологии и психиатрии им. С.С. Корсакова. 2020; 120 (5): 110–5. doi: 10.17116/jnevro2020120051110 [Levin, O.S., Bogolepova A.N. Cognitive rehabilitation of patients with neurodegenerative diseases. Zhurnal nevrologii i psikhiatrii im. S.S. Korsakova. 2020; 120 (5): 110–5]. doi: 10.17116/jnevro2020120051110] (in Russian)].
  8. Feigin V.L., Vos T., Nichols E., Owolabi M.O., Carroll W.M., Dichgans M., Deuschl G., Parmar P., Brainin M., Murray C. The global burden of neurological disorders: translating evidence into policy. Lancet Neurol. 2020; 19 (3): 255–65. doi: 10.1016/S1474-4422(19)30411-9
  9. Воронина Т.А., Белопольская М.В., Хейфец И.А. и др. Изучение действия сверхмалых доз антител к S100 при нарушении когнитивных функций, эмоционального и неврологического статусов в условиях экспериментальной модели Болезни Альцгеймера. Бюл. экспер. биол. и мед. 2009; 148 (8): 174–6. [Voronina T.A., Belopolskaya M.V., Heifets I.A. Study of the effect of ultralow doses of antibodies to S100 in impairment of cognitive functions, emotional and neurological status in the experimental model of Alzheimer’s Disease. Biol. of Expert Biol. and Med. 2009; 148 (8): 174–6 (in Russian)].
  10. Литвиненко И.В. Фундаментальные и методологические аспекты изучения прогрессирующих заболеваний центральной нервной системы. Бюллетень Национального общества по изучению болезни Паркинсона и расстройств движений. 2022; 2: 126–30. doi: 10.24412/2226-079Х-2022-12449 [Litvinenko I.V. Fundamental and methodological aspects of the study of progressive diseases of the central nervous system. Byulleten’ Nacional’nogo obshchestva po izucheniyu bolezni Parkinsona i rasstrojstv dvizhenij. 2022; 2: 126–30. doi: 10.24412/2226-079KH-2022-12449 (in Russian)].
  11. Шпилюкова Ю.А., Шабалина А.А., Ахмадулина Д.Р., Федотова Е.Ю. Опыт использования лабораторных биомаркеров в диагностике нейродегенеративных заболеваний. Бюллетень Национального общества по изучению болезни Паркинсона и расстройств движений. 2022; 2: 227–30. doi: 10.24412/2226-079Х-2022-12474 [Shpilyukova YU.A., Shabalina A.A., Akhmadulina D.R., Fedotova E.YU. Experience of using laboratory biomarkers in the diagnosis of neurodegenerative diseases. Byulleten’ Nacional’nogo obshchestva po izucheniyu bolezni Parkinsona iirasstrojstv dvizhenij. 2022; 2: 227–30. doi: 10.24412/2226-079KH-2022-12474 (in Russian)].
  12. Волкова М.В., Рагино Ю.И. Современные биомаркеры окислительного стресса, оцениваемые методом иммуноферментного анализа. Атеросклероз. 2021; 17 (4): 79–92. doi: 10.52727/2078-256Х-2021-17-4-79-92 [Volkova M.V., Ragino YU.I. Modern biomarkers of oxidative stress estimated by immuno-enzymal analysis. Ateroskleroz. 2021; 17 (4): 79–92. doi: 10.52727/2078-256KH-2021-17-4-79-92 (in Russian)].
  13. Колмакова Т.С., Смирнова О.Б., Белякова Е.И. Антиоксидантные свойства ликвора при дегенеративных заболеваниях мозга. Нейрохимия. 2010; 27 (1): 47–52. [Kolmakova T.S., Smirnova O.B., Belyakova E.I. Antioxidant properties of cerebrospinal fluid in degenerative brain diseases. Nejrokhimiya. 2010; 27 (1): 47–52 (in Russian)].
  14. Колмакова Т.С. Участие ликвора в регуляции деятельности мозга. Журнал фундаментальной медицины и биологии. 2012; 3: 36–40. [Kolmakova T.S. Significance of the liquor in regulation of activity of the brain. Zhurnal fundamental’noj mediciny i biologii. 2012; 3: 36–40 (in Russian)].
  15. Luebke M., Parulekar M., Florian P. Thomas, Fluid biomarkers for the diagnosis of neurodegenerative diseases. Biomarkers in Neuropsychiatry. 2023; 8: 100062. doi: 10.1016/j.bionps.2023.100062
  16. Гончарова З. А., Колмакова Т. С., Оксенюк О.С., Моргуль Е. В., Гельпей М.А., Власова Н.Д., Смирнова О.Б., Муталиева Х.М. Возможные лабораторные и инструментальные маркеры болезни Паркинсона. Саратовский научно-медицинский журнал. 2020; 16 (1): 336–41. DOI: ssmj.ru/en/2020/1/336 [Goncharova Z.A., Kolmakova T.S., Oksenyuk O.S., Morgul E.V., Gelpey M.A., Vlasova N.D., Smirnova O.B., Mutalieva Kh.M. Possible laboratory and instrumental markers of Parkinson’s disease. Saratovskij nauchno-medicinskij zhurnal. 2020; 16 (1): 336–41. DOI: ssmj.ru/en/2020/1/336 (in Russian)].
  17. Mondragón-Rodriguez S., Perry G., Zhu X., Boehm J. Amyloid beta and tau proteins as therapeutic targets for Alzheimer’s disease treatment: rethinking the current strategy. International J. of Alzheimer’s Disease. 2012; 2012: 630182. doi: 10.1155/2012/630182
  18. Ellis G., Fang E., Maheshwari M., Roltsch E., Holcomb L., Zimmer D., Martinez D., Murray I.V. Lipid oxidation and modification of amyloid-β (Aβ) in vitro and in vivo. J. of Alzheimer’s Disease. 2010; 22 (2): 593–607. doi: 10.3233/JAD-2010-100960
  19. Rossi M., Candelise N., Baiardi S., Capellari S., Giannini G., Orrù C.D., Antelmi E., Mammana A., Hughson A.G., Calandra-Buonaura G., Ladogana A., Plazzi G., Cortelli P., Caughey B., Parchi P. Ultrasensitive RT-QuIC assay with high sensitivity and specificity for Lewy body-associated synucleinopathies. Acta Neuropathol. 2020; 140 (1): 49–62. doi: 10.1007/s00401-020-02160-8
  20. Piazza J.R., Almeida D.M., Dmitrieva N.O., Klein L.C. Frontiers in the use of biomarkers of health in research on stress and aging. J. Gerontol B Psychol Sci Soc Sci. 2010; 65 (5): 513–25. doi: 10.1093/geronb/gbq049.
  21. Petrovic S., Arsic A., Ristic-Medic D., Cvetkovic Z., Vucic V. Lipid Peroxidation and Antioxidant Supplementation in Neurodegenerative Diseases: A Review of Human Studies. Antioxidants (Basel). 2020; 9 (11): 1128. doi: 10.3390/antiox9111128
  22. Вилков Г.А., Смирнова О.Б., Межова Л.И. Коррекция нейроиммунных реакций регуляцией перекисного окисления липидов. Бюллетень экспериментальной биологии и медицины. 1993; 116 (10): 364–6. [Vilkov G.A., Smirnova O.B., Mezhova L.I. Correction of neuroimmune reactions by regulation of lipid peroxidation. Byulleten’ ehksperimental’noj biologii i mediciny. 1993; 116 (10): 364–6 (in Russian)].
  23. Челомбитько М.А. Роль активных форм кислорода в воспалении. Мини-обзор. Вестник Московского университета. Серия 16. Биология. 2018; 73 (4): 242–6. [Chelombit’ko M.A. The role of reactive oxygen species in inflammation. Mini-review. Vestnik Moskovskogo universiteta. Seriya 16. Biologiya. 2018; 73 (4): 242–6 (in Russian)].
  24. Miller E., Markiewicz L., Kabzinski J., Odrobina D., Majsterek I. Potential of redox therapies in neurodegenerative disorders. Front Biosci (Elite Ed). 2017; 9 (2): 214–34. doi: 10.2741/e797
  25. Reed T.T. Lipid peroxidation and neurodegenerative disease. Free Radic Biol Med. 2011; 51 (7): 1302–19. doi: 10.1016/j.freeradbiomed.2011.06.027
  26. Domanskyi A., Parlato R. Oxidative stress in neurodegenerative diseases. Antioxidants. 2022; 11 (3): 504. doi: 10.3390/antiox11030504;
  27. Cioffi F., Adam R.H.I., Bansal R., Broersen K. A review of oxidative stress products and related genes in early Alzheimer’s disease. J. of Alzheimer’s Disease. 2021; 83 (3): 977–1001. doi: 10.3233/jad-210497
  28. Савина К.В., Гречун А.А. 4-гидрокси-транс-2-ноненаль – сигнальный биомаркер процессов оксидативного стресса при перекисном окислении липидов. Инновационное развитие и потенциал современной науки: материалы Международной (заочной) научно-практической конференции. Нефтекамск: Научно-издательский центр «Мир науки», 2022; 19–23. [Savina K. V., Grechun A.A. 4-gidroksi-trans-2-nonenal’ – signal’nyj biomarker processov oksidativnogo stressa pri perekisnom okislenii lipidov Innovacionnoe razvitie i potencial sovremennoj nauki: materialy Mezhdunarodnoj (zaochnoj) nauchno-prakticheskoj konferencii. Neftekamsk: Nauchno-izdatel’skij centr «Mir nauki», 2022; 19–23 (in Russian)].
  29. Sidorova Y., Domanskyi A. Detecting oxidative stress biomarkers in neurodegenerative disease models and patients. Methods Protoc. 2020; 3 (4): 66. doi: 10.3390/mps3040066
  30. Fazzini E., Fleming J., Fahn S. Cerebrospinal fluid antibodies to coronavirus in patients with Parkinson’s disease. Mov Disord. 1992; 7 (2): 153–8. doi: 10.1002/mds.870070210
  31. Iacono S., Schirò G., Davi C., Mastrilli S., Abbott M., Guajana F., Arnao V., Aridon P., Ragonese P., Gagliardo C., Colomba C., Scichilone N., D’Amelio M. COVID-19 and neurological disorders: what might connect Parkinson’s disease to SARS-CoV-2 infection. Front Neurol. 2023; 14: 1172416. doi: 10.3389/fneur.2023.1172416
  32. Casetta B., Longini M., Proietti F., Perrone S., Buonocore G. Development of a fast and simple LC-MS/MS method for measuring the F2-isoprostanes in newborns. Journal of Maternal-Fetal and Neonatal Medicine. 2012; 25 (1): 114–8. doi: 10.3109/14767058.2012.664856
  33. Хадзиева Х.И, Черникова И.В., Милютина Н.П., Плотников А.А. Клиническая и биохимическая гетерогенность болезни Паркинсона. Журнал неврологии и психиатрии имени С.С. Корсакова. 2020; 120 (12): 80–5. doi: 10.17116/jnevro202012012180 [Hadzieva KHI, Chernikova I.V., Milyutina N.P., Plotnikov A.A. Clinical and biochemical heterogeneity of Parkinson’s disease. Zhurnal nevrologii i psikhiatrii imeni S.S. Korsakova. 2020; 120 (12): 80–5. doi: 10.17116/jnevro202012012180 (in Russian)].
  34. Briyal S., Ranjan A.K., Gulati A. Oxidative stress: A target to treat Alzheimer’s disease and stroke. Neurochem Int. 2023; 165: 105509. doi: 10.1016/j.neuint.2023.105509
  35. Uddin M.S., Tewari D., Sharma G., Kabir M.T., Barreto G.E., Bin-Jumah M.N., Perveen A., Abdel-Daim M.M., Ashraf G.M. Molecular mechanisms of ER stress and UPR in the pathogenesis of Alzheimer’s disease. Mol. Neurobiol. 2020; 57 (7): 2902–19. doi: 10.1007/s12035-020-01929-y
  36. Grao-Cruces E., Claro-Cala C.M., Montserrat-de la Paz S., Nobrega C. Lipoprotein metabolism, protein aggregation, and Alzheimer’s disease: A literature review. Int. J. Mol. Sci. 2023; 24 (3): 2944. doi: 10.3390/ijms24032944
  37. Sultana R., Perluigi M., Butterfield D.A. Lipid peroxidation triggers neurodegeneration: a redox proteomics view into the Alzheimer disease brain. Free Radic. Biol Med. 2013; 62: 157–69. doi: 10.1016/j.freeradbiomed.2012.09.027
  38. Ashrafian H., Zadeh E.H., Khan R.H. Review on Alzheimer’s disease: Inhibition of amyloid beta and tau tangle formation. Int. J. Biol. Macromol. 2021; 167: 382–94. doi: 10.1016/j.ijbiomac.2020.11.192
  39. Miller E., Walczak A., Saluk J., Ponczek M.B., Majsterek I. Oxidative modification of patient’s plasma proteins and its role in pathogenesis of multiple sclerosis. Clin Biochem. 2012; 45 (1–2): 26–30. doi: 10.1016/j.clinbiochem.2011.09.021
  40. Miller E., Wachowicz B., Majsterek I. Advances in antioxidative therapy of multiple sclerosis. Curr. Med. Chem. 2013; 20 (37): 4720–30. doi: 10.2174/09298673113209990156
  41. Perluigi M., Fai Poon H., Hensley K., Pierce W.M., Klein J.B., Calabrese V., De Marco C., Butterfield D.A. Proteomic analysis of 4-hydroxy-2-nonenal-modified proteins in G93A-SOD1 transgenic mice a model of familial amyotrophic lateral sclerosis. Free Radic. Biol. Med. 2005; 38: 960–8. doi: 10.1074/mcp.M500090-MCP200
  42. D’Amico E., Factor-Litvak P., Santella R.M., Mitsumoto H. Clinical perspective on oxidative stress in sporadic amyotrophic lateral sclerosis. Free Radic Biol Med. 2013; 65: 509–27. doi: 10.1016/j.freeradbiomed.2013.06.029
  43. Hey G., Nair N., Klann E., Gurrala A., Safarpour D., Mai V., Ramirez-Zamora A., Vedam-Mai V. Therapies for Parkinson’s disease and the gut microbiome: evidence for bidirectional connection. Front Aging Neurosci. 2023; 15: 1151850. doi: 10.3389/fnagi.2023.1151850
  44. Agrawal M., Biswas A. Molecular diagnostics of neurodegenerative disorders. Front Mol. Biosci. 2015; 2:54. doi: 10.3389/fmolb.2015.00054
  45. Misko A., Jiang S., Wegorzewska I., Milbrandt J., Baloh R.H. Mitofusin 2 is necessary for transport of axonal mitochondria and interacts with the Miro/Milton complex. J. Neurosci. 2010; 30 (12): 4232–40. doi: 10.1523/JNEUROSCI.6248-09.2010
  46. Tse J.K.Y. Gut Microbiota, Nitric Oxide, and Microglia as Prerequisites for Neurodegenerative Disorders. ACS Chem Neurosci. 2017; 8 (7): 1438–47. doi: 10.1021/acschemneuro.7b00176
  47. Сальков В.Н., Худоерков Р.М. Изменение содержания железа в структурах головного мозга при старении и ассоциированных с ним нейродегенеративных заболеваниях. Архив патологии. 2020; 82 (5): 73–8. [Sal’kov V.N., Khudoerkov R.M. Changes in iron content in brain structures during aging and associated neurodegenerative diseases. Arkhiv patologii. 2020; 82 (5): 73–8. doi: 10.17116/patol20208205173 (in Russian)].
  48. Клименко Л.Л., Скальный А.В., Турна А.А., Деев А.И., Буданова М.Н., Баскаков И.С., Никонорова Е.А. Металло-лигандный гомеостаз в этиопатогенезе болезни Альцгеймера (обзор). Микроэлементы в медицине. 2016; 17 (4): 10–3. doi: 10.19112/2413-6174-2016-17-4-3-10 [Klimenko L.L., Skal’nyj A.V., Turna A.A., Deev A.I., Budanova M.N., Baskakov I.S., Nikonorova E.A. Metal-ligand homeostasis in etiopathogenesis of Alzheimer’s disease (review). 2016; 17 (4): 10–3. doi: 10.19112/2413-6174-2016-17-4-3-10 (in Russian)].
  49. Литвиненко И.В., Красаков И.В., Труфанов А.Г. Церебральные нарушения обмена железа как основа развития и прогрессирования нейродегенеративных заболеваний. Вестник Российской Военно-медицинской академии. 2018; 3 (63): 68–73. [Litvinenko I.V., Krasakov I.V., Trufanov A.G. Cerebral disorders of iron metabolism as a basis for development and progression Neurodegenerative diseases. Vestnik Rossijskoj Voenno-medicinskoj akademii. 2018; 3 (63): 68–73 (in Russian)].
  50. Лукина Е.А., Деженкова А.В. Метаболизм железа в норме и патологии. Клиническая онкогематология. 2015; 8 (4): 355–61. doi: 10.21320/2500-2139-2015-8-4-355-361 [Lukina E.A., Dezhenkova A.V. Iron Metabolism in Normal and Pathological Conditions. Clinical oncohematology. 2015; 8 (4): 355–61. doi: 10.21320/2500-2139-2015-8-4-355-361 (in Russian)].
  51. Аутлев К.М., Кручинин Е.В. Козлов М.В., Мокин Е.А., Ахметьянов М.А., Алекберов Р.И., Лукашенок А.В., Аутлев М.К., Яниева Ю.С. Наследственные нейродегенерации с накоплением железа в мозге. Уральский медицинский журнал. 2019; 3 (171): 9–15. DOI: 10/25694/URMJ.2019.03.15 [Autlev K.M., KruchiniNE.V. Kozlov M.V. Mokin E.A. Akhmetianov M.A., Alekberov R.I., Lukashenok A.V., Autlev M.K., Yanieva Y.S. Hereditary neurodegeneration with iron accumulation in the brain (literature review). Ural’skij medicinskij zhurnal. 2019; 3 (171): 9–15. DOI: 10/25694/URMJ.2019.03.15 (in Russian)].
  52. Буряк А.Б. Труфанов А.Г. Особенности клинического течения болезни Паркинсона при отложении железа в базальных ганглиях. РМЖ. 2022; 4: 2–6. [Buryak A.B. Trufanov A.G. Parkinson’s disease patterns in neurodegeneration with brain iron accumulation. RMZH. 2022; 4: 2–6 (in Russian)].
  53. Яшин А., Яшин Я. Высокоэффективная жидкостная хроматография маркеров окислительного стресса. Аналитика. 2011; 1: 34–47. [Yashin A., Yashin YA. High-performance liquid chromatography of oxidative stress markers. Analitika. 2011; 1: 34–47 (in Russian)].
  54. Milne G.L., Gao B., Terry E.S., Zackert W.E., Sanchez S.C. Measurement of F2-isoprostanes and isofurans using gas chromatography-mass spectrometry. Free Radical Biology and Medicine. 2013; 59: 36–44.

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