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Advanced Oxidative Protein Products Role in Multiple Sclerosis: a Systematic Review and Meta-analysis

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Abstract

Multiple sclerosis (MS) is an autoimmune-mediated disease that damages the central nervous system. MS pathophysiological features are not entirely understood, but the increase of reactive oxygen species (ROS) possibly causes myelin and oligodendrocyte degeneration. ROS-increased production generates new compounds through oxidative modifications, including advanced oxidative protein products (AOPPs). The AOPPs are oxidative stress biomarkers and inflammatory mediators commonly formed by hypochlorous acid oxidative action on albumin. Considering that AOPPs accumulation produces ROS and induces neuronal apoptosis, these may represent a new target for drug development to MS treatment and a possible biomarker to monitor the severity of the disease. Thus, this review aims to investigate if there is an alteration in the AOPPs levels in MS and its possible involvement in patient disability. The second objective is to analyze whether drugs or compounds used in MS treatment could modify the AOPPs levels. The protocol was registered in PROSPERO (CRD42020203268). The databases’ search yielded 327 articles. We excluded 259 duplicated articles and evaluated 68 articles by the title and abstract. We full-text analyzed 17 articles and included 13 articles. The AOPPs levels were increased in not-treated MS patients. Furthermore, the increase in disability status was associated with AOPPs accumulation in not-treated MS patients. Additionally, the AOPPs levels were reduced in MS patients after treatment. Therefore, AOPPs seem to play a role in MS pathophysiology and may become a new target for drug development and help MS diagnosis or treatment follow-up.

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Data and Materials Availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. Lublin FD (2014) New multiple sclerosis phenotypic classification. Eur Neurol 72(Suppl 1):1–5. https://doi.org/10.1159/000367614

    Article  PubMed  Google Scholar 

  2. Katsara M, Apostolopoulos V (2018) Multiple sclerosis: pathogenesis and therapeutics. Med Chem 14(2)

  3. Baecher-Allan C, Kaskow BJ, Weiner HL (2018) Multiple sclerosis: mechanisms and immunotherapy. Neuron 97(4):742–768. https://doi.org/10.1016/j.neuron.2018.01.021

    Article  CAS  PubMed  Google Scholar 

  4. Thompson AJ, Baranzini SE, Geurts J, Hemmer B, Ciccarelli O (2018) Multiple sclerosis. Lancet 391(10130):1622–1636. https://doi.org/10.1016/s0140-6736(18)30481-1

    Article  PubMed  Google Scholar 

  5. Kalincik T (2015) Multiple sclerosis relapses: epidemiology, outcomes and management A Systematic Review. Neuroepidemiology 44(4):199–214. https://doi.org/10.1159/000382130

    Article  PubMed  Google Scholar 

  6. Biernacki T, Sandi D, Fricska-Nagy Z, Kincses ZT, Fuvesi J, Laczko R, Kokas Z, Klivenyi P, Vecsei L, Bencsik K (2020) Epidemiology of multiple sclerosis in Central Europe, update from Hungary. Brain Behav 10(5):1–10. https://doi.org/10.1002/brb3.1598

    Article  Google Scholar 

  7. Lublin FD, Reingold SC, Cohen JA, Cutter GR, Sorensen PS, Thompson AJ, Wolinsky JS, Balcer LJ, Banwell B, Barkhof F, Bebo B Jr, Calabresi PA, Clanet M, Comi G, Fox RJ, Freedman MS, Goodman AD, Inglese M, Kappos L, Kieseier BC, Lincoln JA, Lubetzki C, Miller AE, Montalban X, O’Connor PW, Petkau J, Pozzilli C, Rudick RA, Sormani MP, Stuve O, Waubant E, Polman CH (2014) Defining the clinical course of multiple sclerosis: the 2013 revisions. Neurology 83(3):278–286. https://doi.org/10.1212/WNL.0000000000000560

    Article  PubMed  PubMed Central  Google Scholar 

  8. Harris VK, Tuddenham JF, Sadiq SA (2017) Biomarkers of multiple sclerosis: current findings. Degener Neurol Neuromuscul Dis 7(1):19–29. https://doi.org/10.2147/DNND.S98936

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Confavreux C, Vukusic S, Moreau T, Adeleine P (2000) Relapses and progression of disability in multiple sclerosis. N Engl J Med 343(20):1430–1438. https://doi.org/10.1056/NEJM200011163432001

    Article  CAS  PubMed  Google Scholar 

  10. Zeydan B, Atkinson EJ, Weis DM, Smith CY, Gazzuola Rocca L, Rocca WA, Keegan BM, Weinshenker BG, Kantarci K, Kantarci OH (2020) Reproductive history and progressive multiple sclerosis risk in women. Brain Commun 2(2):fcaa185. https://doi.org/10.1093/braincomms/fcaa185

    Article  PubMed  PubMed Central  Google Scholar 

  11. Chataway J, De Angelis F, Connick P, Parker RA, Plantone D, Doshi A, John N, Stutters J, MacManus D, Prados Carrasco F, Barkhof F, Ourselin S, Braisher M, Ross M, Cranswick G, Pavitt SH, Giovannoni G, Gandini Wheeler-Kingshott CA, Hawkins C, Sharrack B, Bastow R, Weir CJ, Stallard N, Chandran S, Investigators M-S (2020) Efficacy of three neuroprotective drugs in secondary progressive multiple sclerosis (MS-SMART): a phase 2b, multiarm, double-blind, randomised placebo-controlled trial. Lancet Neurol 19(3):214–225. https://doi.org/10.1016/S1474-4422(19)30485-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Correale J, Gaitan MI, Ysrraelit MC, Fiol MP (2017) Progressive multiple sclerosis: from pathogenic mechanisms to treatment. Brain 140(3):527–546. https://doi.org/10.1093/brain/aww258

    Article  PubMed  Google Scholar 

  13. Tintore M, Vidal-Jordana A, Sastre-Garriga J (2019) Treatment of multiple sclerosis - success from bench to bedside. Nat Rev Neurol 15(1):53–58. https://doi.org/10.1038/s41582-018-0082-z

    Article  CAS  PubMed  Google Scholar 

  14. Ontaneda D (2019) Progressive multiple sclerosis. Continuum (Minneap Minn) 25(3):736–752. https://doi.org/10.1212/CON.0000000000000727

    Article  Google Scholar 

  15. Oliveira SR, Kallaur AP, Reiche EMV, Kaimen-Maciel DR, Panis C, Lozovoy MAB, Morimoto HK, Maes M, Dichi I, Simao ANC (2016) Albumin and protein oxidation are predictors that differentiate relapsing-remitting from progressive clinical forms of multiple sclerosis. Mol Neurobiol 54(4):2961–2968. https://doi.org/10.1007/s12035-016-9860-z

    Article  CAS  PubMed  Google Scholar 

  16. Strzepa A, Pritchard KA, Dittel BN (2017) Myeloperoxidase: a new player in autoimmunity. Cell Immunol 317(1):1–8. https://doi.org/10.1016/j.cellimm.2017.05.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Malle E, Furtmuller PG, Sattler W, Obinger C (2007) Myeloperoxidase: a target for new drug development? Br J Pharmacol 152(6):838–854. https://doi.org/10.1038/sj.bjp.0707358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Bochi GV, Torbitz VD, Cargnin LP, de Carvalho JA, Gomes P, Moresco RN (2014) An alternative pathway through the Fenton reaction for the formation of advanced oxidation protein products, a new class of inflammatory mediators. Inflammation 37(2):512–521. https://doi.org/10.1007/s10753-013-9765-1

    Article  CAS  PubMed  Google Scholar 

  19. Choi DK, Koppula S, Choi M, Suk K (2010) Recent developments in the inhibitors of neuroinflammation and neurodegeneration: inflammatory oxidative enzymes as a drug target. Expert Opin Ther Pat 20(11):1531–1546. https://doi.org/10.1517/13543776.2010.525220

    Article  CAS  PubMed  Google Scholar 

  20. Ding R, Sun B, Liu Z, Yao X, Wang H, Shen X, Jiang H, Chen J (2017) Advanced oxidative protein products cause pain hypersensitivity in rats by inducing dorsal root ganglion neurons apoptosis via NADPH oxidase 4/c-Jun N-terminal kinase pathways. Front Mol Neurosci 10(195):1–13. https://doi.org/10.3389/fnmol.2017.00195

    Article  CAS  Google Scholar 

  21. Adamczyk B (2016) Adamczyk-Sowa M (2016) New insights into the role of oxidative stress mechanisms in the pathophysiology and treatment of multiple sclerosis. Oxid Med Cell Longev 1:1–18. https://doi.org/10.1155/2016/1973834

    Article  CAS  Google Scholar 

  22. Shamseer L, Moher D, Clarke M, Ghersi D, Liberati A, Petticrew M, Shekelle P, Stewart LA (2015) Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015: elaboration and explanation. BMJ 350(7647):1–25. https://doi.org/10.1136/bmj.g7647

    Article  Google Scholar 

  23. Munnangi S, Boktor SW (2020) Epidemiology of study design. In Treasure Island: StatPearls

  24. Stang A (2010) Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol 25(9):603–605. https://doi.org/10.1007/s10654-010-9491-z

    Article  PubMed  Google Scholar 

  25. Higgins JP, Altman DG, Gotzsche PC, Juni P, Moher D, Oxman AD, Savovic J, Schulz KF, Weeks L, Sterne JA, Cochrane Bias Methods G, Cochrane Statistical Methods G (2011) The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. BMJ 343(1):1–9. https://doi.org/10.1136/bmj.d5928

    Article  Google Scholar 

  26. DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7(3):177–188. https://doi.org/10.1016/0197-2456(86)90046-2

    Article  CAS  PubMed  Google Scholar 

  27. Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327(7414):557–560. https://doi.org/10.1136/bmj.327.7414.557

    Article  PubMed  PubMed Central  Google Scholar 

  28. Begg CB, Mazumdar M (1994) Operating characteristics of a rank correlation test for publication bias. Biometrics 50(4):1088–1101

    Article  CAS  Google Scholar 

  29. Egger M, Davey Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315(7109):629–634. https://doi.org/10.1136/bmj.315.7109.629

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Sadowska-Bartosz I, Adamczyk-Sowa M, Galiniak S, Mucha S, Pierzchala K, Bartosz G (2013) Oxidative modification of serum proteins in multiple sclerosis. Neurochem Int 63(5):507–516. https://doi.org/10.1016/j.neuint.2013.08.009

    Article  CAS  PubMed  Google Scholar 

  31. Oliveira SR, Simao AN, Kallaur AP, de Almeida ER, Morimoto HK, Lopes J, Dichi I, Kaimen-Maciel DR, Reiche EM (2014) Disability in patients with multiple sclerosis: influence of insulin resistance, adiposity, and oxidative stress. Nutrition 30(3):268–273. https://doi.org/10.1016/j.nut.2013.08.001

    Article  CAS  PubMed  Google Scholar 

  32. Ljubisavljevic S, Stojanovic I, Vojinovic S, Stojanov D, Stojanovic S, Cvetkovic T, Savic D, Pavlovic D (2013) The patients with clinically isolated syndrome and relapsing remitting multiple sclerosis show different levels of advanced protein oxidation products and total thiol content in plasma and CSF. Neurochem Int 62(7):988–997. https://doi.org/10.1016/j.neuint.2013.02.025

    Article  CAS  PubMed  Google Scholar 

  33. Ljubisavljevic S, Stojanovic I, Cvetkovic T, Vojinovic S, Stojanov D, Stojanovic D, Stefanovic N, Pavlovic D (2014) Erythrocytes’ antioxidative capacity as a potential marker of oxidative stress intensity in neuroinflammation. J Neurol Sci 337(1–2):8–13. https://doi.org/10.1016/j.jns.2013.11.006

    Article  CAS  PubMed  Google Scholar 

  34. Pasquali L, Pecori C, Lucchesi C, LoGerfo A, Iudice A, Siciliano G, Bonuccelli U (2015) Plasmatic oxidative stress biomarkers in multiple sclerosis: relation with clinical and demographic characteristics. Clin Biochem 48(1–2):19–23. https://doi.org/10.1016/j.clinbiochem.2014.09.024

    Article  CAS  PubMed  Google Scholar 

  35. Karlik M, Valkovic P, Hancinova V, Krizova L, Tothova L, Celec P (2015) Markers of oxidative stress in plasma and saliva in patients with multiple sclerosis. Clin Biochem 48(1–2):24–28. https://doi.org/10.1016/j.clinbiochem.2014.09.023

    Article  CAS  PubMed  Google Scholar 

  36. Adamczyk-Sowa M, Galiniak S, Zyracka E, Grzesik M, Naparlo K, Sowa P, Bartosz G (2017) Sadowska-Bartosz I (2017) Oxidative modification of blood serum proteins in multiple sclerosis after interferon beta and melatonin treatment. Oxid Med Cell Longev 7905148:1–8. https://doi.org/10.1155/2017/7905148

    Article  CAS  Google Scholar 

  37. Mezzaroba L, Simao ANC, Oliveira SR, Flauzino T, Alfieri DF, de Carvalho Jennings Pereira WL, Kallaur AP, Lozovoy MAB, Kaimen-Maciel DR, Maes M, Reiche EMV (2020) Antioxidant and anti-inflammatory diagnostic biomarkers in multiple sclerosis: a machine learning study. Mol Neurobiol 57(1):2167–2178. https://doi.org/10.1007/s12035-019-01856-7

    Article  CAS  PubMed  Google Scholar 

  38. Oliveira SR, Simao ANC, Alfieri DF, Flauzino T, Kallaur AP, Mezzaroba L, Lozovoy MAB, Sabino BS, Ferreira KPZ, Pereira W, Kaimen-Maciel DR, Dichi I, Reiche EMV (2017) Vitamin D deficiency is associated with disability and disease progression in multiple sclerosis patients independently of oxidative and nitrosative stress. J Neurol Sci 381:213–219. https://doi.org/10.1016/j.jns.2017.07.046

    Article  CAS  PubMed  Google Scholar 

  39. Hányšová S, Čierny D, Petráš M, Lehotský J (2017) Elevated plasma levels of advanced oxidation protein products in Slovak multiple sclerosis patients: possible association with different disability states. Activitas Nervosa Superior Rediviva 59(2):45–50

    Google Scholar 

  40. Sadowska-Bartosz I, Adamczyk-Sowa M, Gajewska A, Bartosz G (2014) Oxidative modification of blood serum proteins in multiple sclerosis after interferon or mitoxantrone treatment. J Neuroimmunol 266(1–2):67–74. https://doi.org/10.1016/j.jneuroim.2013.11.005

    Article  CAS  PubMed  Google Scholar 

  41. Kallaur AP, Reiche EMV, Oliveira SR, Simao ANC, Pereira W, Alfieri DF, Flauzino T, Proenca CM, Lozovoy MAB, Kaimen-Maciel DR, Maes M (2017) Genetic, immune-inflammatory, and oxidative stress biomarkers as predictors for disability and disease progression in multiple sclerosis. Mol Neurobiol 54(1):31–44. https://doi.org/10.1007/s12035-015-9648-6

    Article  CAS  PubMed  Google Scholar 

  42. Pasquali L, Pecori C, Chico L, Iudice A, Siciliano G, Bonuccelli U (2015) Relation between plasmatic and cerebrospinal fluid oxidative stress biomarkers and intrathecal Ig synthesis in multiple sclerosis patients. J Neuroimmunol 283:39–42. https://doi.org/10.1016/j.jneuroim.2015.04.010

    Article  CAS  PubMed  Google Scholar 

  43. Oliveira SR, Kallaur AP, Simao AN, Morimoto HK, Lopes J, Panis C, Petenucci DL, da Silva E, Cecchini R, Kaimen-Maciel DR, Reiche EM (2012) Oxidative stress in multiple sclerosis patients in clinical remission: association with the expanded disability status scale. J Neurol Sci 321(1–2):49–53. https://doi.org/10.1016/j.jns.2012.07.045

    Article  CAS  PubMed  Google Scholar 

  44. Cristani M, Speciale A, Saija A, Gangemi S, Minciullo PL, Cimino F (2016) Circulating advanced oxidation protein products as oxidative stress biomarkers and progression mediators in pathological conditions related to inflammation and immune dysregulation. Curr Med Chem 23(34):3862–3882. https://doi.org/10.2174/0929867323666160902154748

    Article  CAS  PubMed  Google Scholar 

  45. Witko-Sarsat V, Friedlander M, Capeillere-Blandin C, Nguyen-Khoa T, Nguyen AT, Zingraff J, Jungers P, Descamps-Latscha B (1996) Advanced oxidation protein products as a novel marker of oxidative stress in uremia. Kidney Int 49(5):1304–1313. https://doi.org/10.1038/ki.1996.186

    Article  CAS  PubMed  Google Scholar 

  46. Li X, Zhang T, Geng J, Wu Z, Xu L, Liu J, Tian J, Zhou Z, Nie J, Bai X (2019) Advanced oxidation protein products promote lipotoxicity and tubulointerstitial fibrosis via CD36/beta-catenin pathway in diabetic nephropathy. Antioxid Redox Signal 31(7):521–538. https://doi.org/10.1089/ars.2018.7634

    Article  CAS  PubMed  Google Scholar 

  47. Sebekova K, Klenovicsova K, Ferenczova J, Hedvig J, Podracka L, Heidland A (2012) Advanced oxidation protein products and advanced glycation end products in children and adolescents with chronic renal insufficiency. J Ren Nutr 22(1):143–148. https://doi.org/10.1053/j.jrn.2011.10.022

    Article  CAS  PubMed  Google Scholar 

  48. Sciskalska M, Zalewska M, Grzelak A, Milnerowicz H (2014) The influence of the occupational exposure to heavy metals and tobacco smoke on the selected oxidative stress markers in smelters. Biol Trace Elem Res 159(1–3):59–68. https://doi.org/10.1007/s12011-014-9984-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Ibitoye R, Kemp K, Rice C, Hares K, Scolding N, Wilkins A (2016) Oxidative stress-related biomarkers in multiple sclerosis: a review. Biomark Med 10(8):889–902. https://doi.org/10.2217/bmm-2016-0097

    Article  CAS  PubMed  Google Scholar 

  50. Meyer-Moock S, Feng YS, Maeurer M, Dippel FW, Kohlmann T (2014) Systematic literature review and validity evaluation of the Expanded Disability Status Scale (EDSS) and the Multiple Sclerosis Functional Composite (MSFC) in patients with multiple sclerosis. BMC Neurol 14(58):1–10. https://doi.org/10.1186/1471-2377-14-58

    Article  Google Scholar 

  51. Cinar BP, Yorgun YG (2018) What we learned from the history of multiple sclerosis measurement: Expanded Disability Status Scale. Noro Psikiyatr Ars 55(Suppl 1):S69–S75. https://doi.org/10.29399/npa.23343

    Article  PubMed  PubMed Central  Google Scholar 

  52. Torbitz VD, Bochi GV, de Carvalho JA, de Almeida VR, da Silva JE, Moresco RN (2015) In vitro oxidation of fibrinogen promotes functional alterations and formation of advanced oxidation protein products, an inflammation mediator. Inflammation 38(3):1201–1206. https://doi.org/10.1007/s10753-014-0085-x

    Article  CAS  PubMed  Google Scholar 

  53. Lopez-Bascon MA, Priego-Capote F, Peralbo-Molina A, Calderon-Santiago M, Luque de Castro MD (2016) Influence of the collection tube on metabolomic changes in serum and plasma. Talanta 150(1):681–689. https://doi.org/10.1016/j.talanta.2015.12.079

    Article  CAS  PubMed  Google Scholar 

  54. Zadeh AR, Askari M, Azadani NN, Ataei A, Ghadimi K, Tavoosi N, Falahatian M (2019) Mechanism and adverse effects of multiple sclerosis drugs: a review article. Part 1. Int J Physiol Pathophysiol Pharmacol 11(4):95–104

    CAS  Google Scholar 

  55. Dumitrescu L, Constantinescu CS, Tanasescu R (2018) Recent developments in interferon-based therapies for multiple sclerosis. Expert Opin Biol Ther 18(6):665–680. https://doi.org/10.1080/14712598.2018.1462793

    Article  CAS  PubMed  Google Scholar 

  56. Jakimovski D, Kolb C, Ramanathan M, Zivadinov R, Weinstock-Guttman B (2018) Interferon beta for multiple sclerosis. Cold Spring Harb Perspect Med 8(11):1–20. https://doi.org/10.1101/cshperspect.a032003

    Article  CAS  Google Scholar 

  57. Gholamzad M, Ebtekar M, Ardestani MS, Azimi M, Mahmodi Z, Mousavi MJ, Aslani S (2019) A comprehensive review on the treatment approaches of multiple sclerosis: currently and in the future. Inflamm Res 68(1):25–38. https://doi.org/10.1007/s00011-018-1185-0

    Article  CAS  PubMed  Google Scholar 

  58. Wawrzyniak S, Rzepinski L (2020) Is there a new place for mitoxantrone in the treatment of multiple sclerosis? Neurol Neurochir Pol 54(1):54–61. https://doi.org/10.5603/PJNNS.a2019.0069

    Article  PubMed  Google Scholar 

  59. Zadeh AR, Ghadimi K, Ataei A, Askari M, Sheikhinia N, Tavoosi N, Falahatian M (2019) Mechanism and adverse effects of multiple sclerosis drugs: a review article. Part 2. Int J Physiol Pathophysiol Pharmacol 11(4):105–114

    CAS  Google Scholar 

  60. Thompson SG (1994) Why sources of heterogeneity in meta-analysis should be investigated. BMJ 309(6965):1351–1355. https://doi.org/10.1136/bmj.309.6965.1351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Faissner S, Plemel JR, Gold R, Yong VW (2019) Progressive multiple sclerosis: from pathophysiology to therapeutic strategies. Nat Rev Drug Discov 18(12):905–922. https://doi.org/10.1038/s41573-019-0035-2

    Article  CAS  PubMed  Google Scholar 

  62. Saleem S, Anwar A, Fayyaz M, Anwer F, Anwar F (2019) An overview of therapeutic options in relapsing-remitting multiple sclerosis. Cureus 11(7):1–11. https://doi.org/10.7759/cureus.5246

    Article  Google Scholar 

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Acknowledgements

We want to thank Dr. Fabricio B. Zanatta for his help in performing the bias analyses.

Funding

Fellowships from the Conselho Nacional de Desenvolvimento Científico (CNPq) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) are also acknowledged (Ph.D. fellowship to P.R from CAPES [process #88887.501568/2020–00]). G.T is a recipient of a fellowship from CNPq [process #303531/2020–7] and L’ORÉAL-ABC-UNESCO Para Mulheres na Ciência, 2016, and Prêmio Capes de Teses—Ciências Biológicas II, CAPES, 2014 [process #23038.006930/2014/59].

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  1. Graduated Program in Pharmacology, Federal University of Santa Maria (UFSM), Avenida Roraima, 1000, Building 21, Room 5207, Santa Maria, RS, 97105-900, Brazil

    Patrícia Rodrigues, Guilherme Vargas Bochi & Gabriela Trevisan

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PR and GT participated in search design and performed the literature search. PR, GT, and GVB performed data extraction. PR performed data analysis. PR, GT, and GVB wrote or contributed to the writing of the manuscript, and performed the literature search. All authors have read the manuscript and approved the final version of the manuscript.

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Correspondence to Gabriela Trevisan.

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Rodrigues, P., Bochi, G.V. & Trevisan, G. Advanced Oxidative Protein Products Role in Multiple Sclerosis: a Systematic Review and Meta-analysis. Mol Neurobiol 58, 5724–5742 (2021). https://doi.org/10.1007/s12035-021-02493-9

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