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Erschienen in: Neurological Sciences 6/2021

08.10.2020 | Original Article

The correlation between circulating inflammatory, oxidative stress, and neurotrophic factors level with the cognitive outcomes in multiple sclerosis patients

verfasst von: Mahnaz Talebi, Alireza Majdi, Ehsan Nasiri, Amirreza Naseri, Saeed Sadigh-Eteghad

Erschienen in: Neurological Sciences | Ausgabe 6/2021

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Abstract

Introduction

Changes in the levels of circulating markers of inflammation, oxidative stress, and neurotrophic factors might be a good candidate for the prediction of cognitive impairment in multiple sclerosis (MS). Here, the correlation between the mentioned circulating markers with the Cambridge neuropsychological test automated battery (CANTAB) task outcomes was determined in MS patients.

Methods

The CANTAB (paired-associate learning (PAL), reaction time (RTI), rapid visual information processing (RVP), and spatial working memory tasks (SWM)) was completed by the patients. Accordingly, the serum levels of interferon-γ (INF-γ), C-reactive protein (CRP), ciliary neurotrophic factor (CNTF), glial cell line–derived neurotrophic factor (GDNF), and brain-derived neurotrophic factor (BDNF), malondialdehyde (MDA), total antioxidant capacity (TAC), and the acetylcholine esterase (AChE) activity were measured. Cognitive impairment status and the correlation between the circulating factors with the CANTAB outcomes were determined.

Results

The cognitively impaired (CI) patients appropriately differentiated from not cognitively impaired (NCI) ones using the CANTAB tasks. The serum levels of MDA, TAC, CRP, INF-γ, and GDNF correlated with the cognitive scores in MS patients (p < 0.05). After adjusting for age, sex, disease duration, and disability levels (covariates in a regression model), the MDA, INF-γ, and GDNF factors levels were statistically different between CI and NCI groups (p < 0.05).

Discussion

The mentioned markers might predict the cognitive impairment progress and be used as an index of its detection, in addition to neuropsychological assessments, in MS patients.
Literatur
1.
Zurück zum Zitat Arya R, Roth C, Leach JL, Middeler D, Wilson JA, Vannest J, Rozhkov L, Greiner HM, Buroker J, Scholle C, Fujiwara H, Horn PS, Rose DF, Crone NE, Mangano FT, Byars AW, Holland KD (2019) Neuropsychological outcomes after resection of cortical sites with visual naming associated electrocorticographic high-gamma modulation. Epilepsy Res 151:17–23CrossRef Arya R, Roth C, Leach JL, Middeler D, Wilson JA, Vannest J, Rozhkov L, Greiner HM, Buroker J, Scholle C, Fujiwara H, Horn PS, Rose DF, Crone NE, Mangano FT, Byars AW, Holland KD (2019) Neuropsychological outcomes after resection of cortical sites with visual naming associated electrocorticographic high-gamma modulation. Epilepsy Res 151:17–23CrossRef
2.
Zurück zum Zitat Bai Z, Chen D, Wang L, Zhao Y, Liu T, Yu Y, Yan T, Cheng Y (2019) Cerebrospinal fluid and blood cytokines as biomarkers for multiple sclerosis: a systematic review and meta-analysis of 226 studies with 13,526 multiple sclerosis patients. Front Neurosci 13:1026–1026CrossRef Bai Z, Chen D, Wang L, Zhao Y, Liu T, Yu Y, Yan T, Cheng Y (2019) Cerebrospinal fluid and blood cytokines as biomarkers for multiple sclerosis: a systematic review and meta-analysis of 226 studies with 13,526 multiple sclerosis patients. Front Neurosci 13:1026–1026CrossRef
3.
Zurück zum Zitat Benedict RHB, DeLuca J, Enzinger C, Geurts JJG, Krupp LB, Rao SM (2017) Neuropsychology of multiple sclerosis: looking back and moving forward. J Int Neuropsychol Soc 23:832–842CrossRef Benedict RHB, DeLuca J, Enzinger C, Geurts JJG, Krupp LB, Rao SM (2017) Neuropsychology of multiple sclerosis: looking back and moving forward. J Int Neuropsychol Soc 23:832–842CrossRef
4.
Zurück zum Zitat Budni J, Bellettini-Santos T, Mina F, Garcez ML, Zugno AI (2015) The involvement of BDNF, NGF and GDNF in aging and Alzheimer’s disease. Aging Dis 6:331–341CrossRef Budni J, Bellettini-Santos T, Mina F, Garcez ML, Zugno AI (2015) The involvement of BDNF, NGF and GDNF in aging and Alzheimer’s disease. Aging Dis 6:331–341CrossRef
5.
Zurück zum Zitat Cabeça HLS, Rocha LC, Sabbá AF, Tomás AM, Bento-Torres NVO, Anthony DC, Diniz CWP (2018) The subtleties of cognitive decline in multiple sclerosis: an exploratory study using hierarchichal cluster analysis of CANTAB results. BMC Neurol 18:140–140CrossRef Cabeça HLS, Rocha LC, Sabbá AF, Tomás AM, Bento-Torres NVO, Anthony DC, Diniz CWP (2018) The subtleties of cognitive decline in multiple sclerosis: an exploratory study using hierarchichal cluster analysis of CANTAB results. BMC Neurol 18:140–140CrossRef
6.
Zurück zum Zitat Chiapinotto Spiazzi C, Bucco Soares M, Pinto Izaguirry A, Musacchio Vargas L, Zanchi MM, Frasson Pavin N, Ferreira Affeldt R, Seibert Lüdtke D, Prigol M, Santos FW (2015) Selenofuranoside ameliorates memory loss in Alzheimer-like sporadic dementia: AChE activity, oxidative stress, and inflammation involvement. Oxidative Med Cell Longev 2015:976908CrossRef Chiapinotto Spiazzi C, Bucco Soares M, Pinto Izaguirry A, Musacchio Vargas L, Zanchi MM, Frasson Pavin N, Ferreira Affeldt R, Seibert Lüdtke D, Prigol M, Santos FW (2015) Selenofuranoside ameliorates memory loss in Alzheimer-like sporadic dementia: AChE activity, oxidative stress, and inflammation involvement. Oxidative Med Cell Longev 2015:976908CrossRef
7.
Zurück zum Zitat DeLuca GC, Yates RL, Beale H, Morrow SA (2015) Cognitive impairment in multiple sclerosis: clinical, radiologic and pathologic insights. Brain Pathol 25:79–98CrossRef DeLuca GC, Yates RL, Beale H, Morrow SA (2015) Cognitive impairment in multiple sclerosis: clinical, radiologic and pathologic insights. Brain Pathol 25:79–98CrossRef
8.
Zurück zum Zitat Dutta R, McDonough J, Chang A, Swamy L, Siu A, Kidd GJ, Rudick R, Mirnics K, Trapp BD (2007) Activation of the ciliary neurotrophic factor (CNTF) signalling pathway in cortical neurons of multiple sclerosis patients. Brain 130:2566–2576CrossRef Dutta R, McDonough J, Chang A, Swamy L, Siu A, Kidd GJ, Rudick R, Mirnics K, Trapp BD (2007) Activation of the ciliary neurotrophic factor (CNTF) signalling pathway in cortical neurons of multiple sclerosis patients. Brain 130:2566–2576CrossRef
9.
Zurück zum Zitat Emerich DF, Cain CK, Greco C, Saydoff JA, Yi Hu Z, Liu H, Lindner MD (1997) Cellular delivery of human CNTF prevents motor and cognitive dysfunction in a rodent model of Huntington’s disease. Cell Transplant 6:249–266CrossRef Emerich DF, Cain CK, Greco C, Saydoff JA, Yi Hu Z, Liu H, Lindner MD (1997) Cellular delivery of human CNTF prevents motor and cognitive dysfunction in a rodent model of Huntington’s disease. Cell Transplant 6:249–266CrossRef
10.
Zurück zum Zitat Flachenecker P, Müller G, König H, Meissner H, Toyka KV, Rieckmann P (2006) “Fatigue” bei Multipler Sklerose. Nervenarzt 77:165–174CrossRef Flachenecker P, Müller G, König H, Meissner H, Toyka KV, Rieckmann P (2006) “Fatigue” bei Multipler Sklerose. Nervenarzt 77:165–174CrossRef
11.
Zurück zum Zitat Ghassemzadeh H, Mojtabai R, Karamghadiri N, Ebrahimkhani N (2005) Psychometric properties of a Persian-language version of the Beck Depression Inventory-Second edition: BDI-II-PERSIAN. Depress Anxiety 21:185–192CrossRef Ghassemzadeh H, Mojtabai R, Karamghadiri N, Ebrahimkhani N (2005) Psychometric properties of a Persian-language version of the Beck Depression Inventory-Second edition: BDI-II-PERSIAN. Depress Anxiety 21:185–192CrossRef
12.
Zurück zum Zitat Gromisch ES, Portnoy JG, Foley FW (2018) Comparison of the abbreviated minimal assessment of cognitive function in multiple sclerosis (aMACFIMS) and the brief international cognitive assessment for multiple sclerosis (BICAMS). J Neurol Sci 388:70–75CrossRef Gromisch ES, Portnoy JG, Foley FW (2018) Comparison of the abbreviated minimal assessment of cognitive function in multiple sclerosis (aMACFIMS) and the brief international cognitive assessment for multiple sclerosis (BICAMS). J Neurol Sci 388:70–75CrossRef
13.
Zurück zum Zitat Grzegorski T, Losy J (2017) Cognitive impairment in multiple sclerosis - a review of current knowledge and recent research. Rev Neurosci 28:845–860CrossRef Grzegorski T, Losy J (2017) Cognitive impairment in multiple sclerosis - a review of current knowledge and recent research. Rev Neurosci 28:845–860CrossRef
14.
Zurück zum Zitat Guimarães J, Sá MJ (2012) Cognitive dysfunction in multiple sclerosis. Front Neurol 3:74–74CrossRef Guimarães J, Sá MJ (2012) Cognitive dysfunction in multiple sclerosis. Front Neurol 3:74–74CrossRef
15.
Zurück zum Zitat Haider L, Simeonidou C, Steinberger G, Hametner S, Grigoriadis N, Deretzi G, Kovacs GG, Kutzelnigg A, Lassmann H, Frischer JM (2014) Multiple sclerosis deep grey matter: the relation between demyelination, neurodegeneration, inflammation and iron. J Neurol Neurosur PS 85:1386–1395CrossRef Haider L, Simeonidou C, Steinberger G, Hametner S, Grigoriadis N, Deretzi G, Kovacs GG, Kutzelnigg A, Lassmann H, Frischer JM (2014) Multiple sclerosis deep grey matter: the relation between demyelination, neurodegeneration, inflammation and iron. J Neurol Neurosur PS 85:1386–1395CrossRef
16.
Zurück zum Zitat Heldner MR, Kaufmann-Ezra S, Gutbrod K, Bernasconi C, Bigi S, Blatter V, Mattle HP, Müri RM, Verma RK, Kamm CP (2017) Behavioral changes in patients with multiple sclerosis. Front Neurol 8:437–437CrossRef Heldner MR, Kaufmann-Ezra S, Gutbrod K, Bernasconi C, Bigi S, Blatter V, Mattle HP, Müri RM, Verma RK, Kamm CP (2017) Behavioral changes in patients with multiple sclerosis. Front Neurol 8:437–437CrossRef
17.
Zurück zum Zitat Herranz E, Louapre C, Treaba CA, Govindarajan ST, Ouellette R, Mangeat G, Loggia ML, Cohen-Adad J, Klawiter EC, Sloane JA, Mainero C (2019) Profiles of cortical inflammation in multiple sclerosis by 11C-PBR28 MR-PET and 7 Tesla imaging. Mult Scler J:1352458519867320 Herranz E, Louapre C, Treaba CA, Govindarajan ST, Ouellette R, Mangeat G, Loggia ML, Cohen-Adad J, Klawiter EC, Sloane JA, Mainero C (2019) Profiles of cortical inflammation in multiple sclerosis by 11C-PBR28 MR-PET and 7 Tesla imaging. Mult Scler J:1352458519867320
18.
Zurück zum Zitat Hohlfeld R, Kerschensteiner M, Stadelmann C, Lassmann H, Wekerle H (2006) The neuroprotective effect of inflammation: implications for the therapy of multiple sclerosis. Neurol Sci 27:s1–s7CrossRef Hohlfeld R, Kerschensteiner M, Stadelmann C, Lassmann H, Wekerle H (2006) The neuroprotective effect of inflammation: implications for the therapy of multiple sclerosis. Neurol Sci 27:s1–s7CrossRef
19.
Zurück zum Zitat Jana M, Pahan K (2005) Redox regulation of cytokine-mediated inhibition of myelin gene expression in human primary oligodendrocytes. Free Radic Biol Med 39:823–831CrossRef Jana M, Pahan K (2005) Redox regulation of cytokine-mediated inhibition of myelin gene expression in human primary oligodendrocytes. Free Radic Biol Med 39:823–831CrossRef
20.
Zurück zum Zitat Kalb R, Beier M, Benedict RH, Charvet L, Costello K, Feinstein A, Gingold J, Goverover Y, Halper J, Harris C, Kostich L, Krupp L, Lathi E, LaRocca N, Thrower B, DeLuca J (2018) Recommendations for cognitive screening and management in multiple sclerosis care. Mult Scler 24:1665–1680CrossRef Kalb R, Beier M, Benedict RH, Charvet L, Costello K, Feinstein A, Gingold J, Goverover Y, Halper J, Harris C, Kostich L, Krupp L, Lathi E, LaRocca N, Thrower B, DeLuca J (2018) Recommendations for cognitive screening and management in multiple sclerosis care. Mult Scler 24:1665–1680CrossRef
21.
Zurück zum Zitat Kerschensteiner M, Stadelmann C, Dechant G, Wekerle H, Hohlfeld R (2003) Neurotrophic cross-talk between the nervous and immune systems: implications for neurological diseases. Ann Neurol 53:292–304CrossRef Kerschensteiner M, Stadelmann C, Dechant G, Wekerle H, Hohlfeld R (2003) Neurotrophic cross-talk between the nervous and immune systems: implications for neurological diseases. Ann Neurol 53:292–304CrossRef
22.
Zurück zum Zitat Kim DY, Hao J, Liu R, Turner G, Shi F-D, Rho JM (2012) Inflammation-mediated memory dysfunction and effects of a ketogenic diet in a murine model of multiple sclerosis. PLoS One 7:e35476-e35476CrossRef Kim DY, Hao J, Liu R, Turner G, Shi F-D, Rho JM (2012) Inflammation-mediated memory dysfunction and effects of a ketogenic diet in a murine model of multiple sclerosis. PLoS One 7:e35476-e35476CrossRef
23.
Zurück zum Zitat Macías Islas MÁ, Ciampi E (2019) Assessment and impact of cognitive impairment in multiple sclerosis: an overview. Biomedicines 7:22CrossRef Macías Islas MÁ, Ciampi E (2019) Assessment and impact of cognitive impairment in multiple sclerosis: an overview. Biomedicines 7:22CrossRef
24.
Zurück zum Zitat Mancini A, Gaetani L, Di Gregorio M, Tozzi A, Ghiglieri V, Calabresi P, Di Filippo M (2017) Hippocampal neuroplasticity and inflammation: relevance for multiple sclerosis. Mult Scler Demyelinating Disord 2:2CrossRef Mancini A, Gaetani L, Di Gregorio M, Tozzi A, Ghiglieri V, Calabresi P, Di Filippo M (2017) Hippocampal neuroplasticity and inflammation: relevance for multiple sclerosis. Mult Scler Demyelinating Disord 2:2CrossRef
25.
Zurück zum Zitat Marksteiner J, Kemmler G, Weiss EM, Knaus G, Ullrich C, Mechtcheriakov S, Oberbauer H, Auffinger S, Hinterhölzl J, Hinterhuber H, Humpel C (2011) Five out of 16 plasma signaling proteins are enhanced in plasma of patients with mild cognitive impairment and Alzheimer’s disease. Neurobiol Aging 32:539–540CrossRef Marksteiner J, Kemmler G, Weiss EM, Knaus G, Ullrich C, Mechtcheriakov S, Oberbauer H, Auffinger S, Hinterhölzl J, Hinterhuber H, Humpel C (2011) Five out of 16 plasma signaling proteins are enhanced in plasma of patients with mild cognitive impairment and Alzheimer’s disease. Neurobiol Aging 32:539–540CrossRef
26.
Zurück zum Zitat Patanella AK, Zinno M, Quaranta D, Nociti V, Frisullo G, Gainotti G, Tonali PA, Batocchi AP, Marra C (2010) Correlations between peripheral blood mononuclear cell production of BDNF, TNF-alpha, IL-6, IL-10 and cognitive performances in multiple sclerosis patients. J Neurosci Res 88:1106–1112PubMed Patanella AK, Zinno M, Quaranta D, Nociti V, Frisullo G, Gainotti G, Tonali PA, Batocchi AP, Marra C (2010) Correlations between peripheral blood mononuclear cell production of BDNF, TNF-alpha, IL-6, IL-10 and cognitive performances in multiple sclerosis patients. J Neurosci Res 88:1106–1112PubMed
27.
Zurück zum Zitat Polman CH, Wolinsky JS, Reingold SC (2005) Multiple sclerosis diagnostic criteria: three years later. Mult Scler 11:5–12CrossRef Polman CH, Wolinsky JS, Reingold SC (2005) Multiple sclerosis diagnostic criteria: three years later. Mult Scler 11:5–12CrossRef
28.
Zurück zum Zitat Sacco R, Bussman R, Oesch P, Kesselring J, Beer S (2011) Assessment of gait parameters and fatigue in MS patients during inpatient rehabilitation: a pilot trial. J Neurol 258:889–894CrossRef Sacco R, Bussman R, Oesch P, Kesselring J, Beer S (2011) Assessment of gait parameters and fatigue in MS patients during inpatient rehabilitation: a pilot trial. J Neurol 258:889–894CrossRef
29.
Zurück zum Zitat Sarchielli P, Zaffaroni M, Floridi A, Greco L, Candeliere A, Mattioni A, Tenaglia S, Di Filippo M, Calabresi P (2007) Production of brain-derived neurotrophic factor by mononuclear cells of patients with multiple sclerosis treated with glatiramer acetate, interferon-β 1a, and high doses of immunoglobulins. Mult Scler J 13:313–331CrossRef Sarchielli P, Zaffaroni M, Floridi A, Greco L, Candeliere A, Mattioni A, Tenaglia S, Di Filippo M, Calabresi P (2007) Production of brain-derived neurotrophic factor by mononuclear cells of patients with multiple sclerosis treated with glatiramer acetate, interferon-β 1a, and high doses of immunoglobulins. Mult Scler J 13:313–331CrossRef
30.
Zurück zum Zitat Talebi M, Majdi A, Kamari F, Sadigh-Eteghad S (2020) The Cambridge Neuropsychological Test Automated Battery (CANTAB) Versus the Minimal Assessment of Cognitive Function in Multiple Sclerosis (MACFIMS) for the assessment of cognitive function in patients with multiple sclerosis. Mult Scler Relat Disord:102172 Talebi M, Majdi A, Kamari F, Sadigh-Eteghad S (2020) The Cambridge Neuropsychological Test Automated Battery (CANTAB) Versus the Minimal Assessment of Cognitive Function in Multiple Sclerosis (MACFIMS) for the assessment of cognitive function in patients with multiple sclerosis. Mult Scler Relat Disord:102172
31.
Zurück zum Zitat Tasset I, Agüera E, Sánchez-López F, Feijóo M, Giraldo AI, Cruz AH, Gascón F, Túnez I (2012) Peripheral oxidative stress in relapsing–remitting multiple sclerosis. Clin Biochem 45:440–444CrossRef Tasset I, Agüera E, Sánchez-López F, Feijóo M, Giraldo AI, Cruz AH, Gascón F, Túnez I (2012) Peripheral oxidative stress in relapsing–remitting multiple sclerosis. Clin Biochem 45:440–444CrossRef
32.
Zurück zum Zitat van Horssen J, Schreibelt G, Drexhage J, Hazes T, Dijkstra CD, van der Valk P, de Vries HE (2008) Severe oxidative damage in multiple sclerosis lesions coincides with enhanced antioxidant enzyme expression. Free Radic Biol Med 45:1729–1737CrossRef van Horssen J, Schreibelt G, Drexhage J, Hazes T, Dijkstra CD, van der Valk P, de Vries HE (2008) Severe oxidative damage in multiple sclerosis lesions coincides with enhanced antioxidant enzyme expression. Free Radic Biol Med 45:1729–1737CrossRef
Metadaten
Titel
The correlation between circulating inflammatory, oxidative stress, and neurotrophic factors level with the cognitive outcomes in multiple sclerosis patients
verfasst von
Mahnaz Talebi
Alireza Majdi
Ehsan Nasiri
Amirreza Naseri
Saeed Sadigh-Eteghad
Publikationsdatum
08.10.2020
Verlag
Springer International Publishing
Erschienen in
Neurological Sciences / Ausgabe 6/2021
Print ISSN: 1590-1874
Elektronische ISSN: 1590-3478
DOI
https://doi.org/10.1007/s10072-020-04807-6

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