Document Type : Original Article

Authors

Multiple Sclerosis Research Center, Neuroscience Institute, Tehran University of Medical Sciences, Tehran, Iran

Abstract

Background: Cognitive dysfunction is one of the problems that patients with neuromyelitis optica spectrum disorder (NMOSD) suffer from. We aimed to assess the association between demographic and clinical features as well as body mass index (BMI) and cognitive function in patients with NMOSD.
Methods: A cross-sectional study was performed on 41 patients with definite diagnosis of NMOSD. Serum status of neuromyelitis optica immunoglobulin G (NMO-IgG) was determined using enzyme-linked immunosorbent assay (ELISA) method. Cognitive function was assessed by Minimal Assessment of Cognitive Function in Multiple Sclerosis (MACFIMS) battery which is validated for Persian people before and North American Adult Reading Test (NAART).
Results: The mean score of NAART test was higher in participants with normal weight compared with overweight patients (40.47 ± 3.51 vs. 36.00 ± 5.74, P = 0.02). Current age was negatively correlated with Delis-Kaplan Executive Function System (D-KEFS)-Sorting (P = 0.05, r = -0.30). The correlation of duration of disease and cognitive performance was not significant (P > 0.05). Higher physical disability based on Expanded Disability Status Scale (EDSS) was correlated with lower results in Brief Visuospatial Memory Test-Revised (BVMT-R) (P < 0.01, r = -0.50), California Verbal Learning Test-second edition (CVLT-II)-Delayed Recall (P = 0.02, r = -0.35), and Symbol Digit Modalities Test (SDMT) (P = 0.03, r = -0.33) subtests of MACFIMS. Annual relapse rate was indirectly correlated with CVLT-II (P = 0.03, r = -0.34) and CVLT-II-Delayed Recall (P = 0.01, r = -0.38). Male participants obtained better scores in Paced Auditory Serial Addition Test (PASAT) subtest (P = 0.05). NMO-IgG seropositive patients had poorer performance in terms of CVLT-II-Delayed Recall, Controlled Oral Word Association Test (COWAT), and D-KEFS-Descriptive (P < 0.05). Participants with bachelor and master education degrees showed significantly better results compared to those with high school degree (P < 0.05).
Conclusion: Investigating the clinical and demographic factors affecting cognitive impairment can increase the awareness of health care providers for early diagnosis of cognitive impairment in patients with NMOSD and increase the quality of health services.

Keywords

  1. Holroyd KB, Manzano GS, Levy M. Update on neuromyelitis optica spectrum disorder. Curr Opin Ophthalmol 2020; 31(6): 462-8.
  2. Oh J, Levy M. Neuromyelitis optica: An antibody-mediated disorder of the central nervous system. Neurol Res Int 2012; 2012: 460825.
  3. Wingerchuk DM, Banwell B, Bennett JL, Cabre P, Carroll W, Chitnis T, et al. International consensus diagnostic criteria for neuromyelitis optica spectrum disorders. Neurology 2015; 85(2): 177-89.
  4. Rezaeimanesh N, Sahraian MA, Moghadasi AN, Eskandarieh S. Epidemiology of neuromyelitis optica spectrum disorder in Tehran, Iran: The prevalence, baseline characteristics, and clinical aspects. Neurol Sci 2020; 41(9): 2647-8.
  5. Uzawa A, Mori M, Kuwabara S. Cytokines and chemokines in neuromyelitis optica: pathogenetic and therapeutic implications. Brain Pathol 2014; 24(1): 67-73.
  6. Wang KC, Lee CL, Chen SY, Chen JC, Yang CW, Chen SJ, et al. Distinct serum cytokine profiles in neuromyelitis optica and multiple sclerosis. J Interferon Cytokine Res 2013; 33(2): 58-64.
  7. Meng H, Xu J, Pan C, Cheng J, Hu Y, Hong Y, et al. Cognitive dysfunction in adult patients with neuromyelitis optica: A systematic review and meta-analysis.
    J Neurol 2017; 264(8): 1549-58.
  8. Moghadasi AN, Mirmosayyeb O, Mohammadi A, Sahraian MA, Ghajarzadeh M. The prevalence of cognitive impairment in patients with neuromyelitis optica spectrum disorders (NMOSD): A systematic review and meta-analysis. Mult Scler Relat Disord 2021; 49: 102757.
  9. Jarius S, Ruprecht K, Wildemann B, Kuempfel T, Ringelstein M, Geis C, et al. Contrasting disease patterns in seropositive and seronegative neuromyelitis optica: A multicentre study of 175 patients. J Neuroinflammation. 2012; 9(1): 14.
  10. Czarnecka D, Oset M, Karlinska I, Stasiolek M. Cognitive impairment in NMOSD-More questions than answers. Brain Behav 2020; 10(11): e01842.
  11. Scharfman HE, Binder DK. Aquaporin-4 water channels and synaptic plasticity in the hippocampus. Neurochem Int 2013; 63(7): 702-11.
  12. Fan Y, Liu M, Wu X, Wang F, Ding J, Chen J, et al. Aquaporin-4 promotes memory consolidation in Morris water maze. Brain Struct Funct 2013; 218(1): 39-50.
  13. Saji E, Arakawa M, Yanagawa K, Toyoshima Y, Yokoseki A, Okamoto K, et al. Cognitive impairment and cortical degeneration in neuromyelitis optica. Ann Neurol 2013; 73(1): 65-76.
  14. Qu Y, Hu HY, Ou YN, Shen XN, Xu W, Wang ZT, et al. Association of body mass index with risk of cognitive impairment and dementia: A systematic review and meta-analysis of prospective studies. Neurosci Biobehav Rev 2020; 115: 189-98.
  15. Owji M, Ashraf-Ganjouei A, Sahraian MA, Bidadian M, Ghadiri F, Naser MA. The relationship between cognitive function and body mass index in multiple sclerosis patients. Mult Scler Relat Disord 2019; 32: 37-40.
  16. World Health Organization. Body Mass Index - BMI [Online]. [cited 2022]; Available from: URL: https://www.euro.who.int/en/health-topics/disease-prevention/nutrition/a-healthy-lifestyle/body-mass-index-bmi
  17. Eshaghi A, Riyahi-Alam S, Roostaei T, Haeri G, Aghsaei A, Aidi MR, et al. Validity and reliability of a Persian translation of the Minimal Assessment of Cognitive Function in Multiple Sclerosis (MACFIMS). Clin Neuropsychol 2012; 26(6): 975-84.
  18. Alirezaei M, Forouzannia SM, Yarahmadi P, Sahraian MA, Owji M, Bidadian M, et al. Demographic features, behavioral measures, and clinical factors as predictors of cognitive function in patients with multiple sclerosis. Mult Scler Relat Disord 2021; 49: 102758.
  19. Vanotti S, Cores EV, Eizaguirre B, Melamud L, Rey R, Villa A. Cognitive performance of neuromyelitis optica patients: comparison with multiple sclerosis. Arq Neuropsiquiatr 2013; 71(6): 357-61.
  20. Hollinger KR, Franke C, Arenivas A, Woods SR, Mealy MA, Levy M, et al. Cognition, mood, and purpose in life in neuromyelitis optica spectrum disorder. J Neurol Sci 2016; 362: 85-90.
  21. Makkar SR, Lipnicki DM, Crawford JD, Kochan NA, Castro-Costa E, Lima-Costa MF, et al. Education and the moderating roles of age, sex, ethnicity and apolipoprotein epsilon 4 on the risk of cognitive impairment. Arch Gerontol Geriatr 2020; 91: 104112.
  22. Sherwin BB. Estrogen and cognitive functioning in women: Lessons we have learned. Behav Neurosci 2012; 126(1): 123-7.
  23. Okamoto S, Kobayashi E, Murayama H, Liang J, Fukaya T, Shinkai S. Decomposition of gender differences in cognitive functioning: National Survey of the Japanese elderly. BMC Geriatr 2021; 21(1): 38.
  24. Barrett-Connor E, Kritz-Silverstein D. Gender differences in cognitive function with age: The Rancho Bernardo study. J Am Geriatr Soc 1999; 47(2): 159-64.
  25. Skucas VA, Mathews IB, Yang J, Cheng Q, Treister A, Duffy AM, et al. Impairment of select forms of spatial memory and neurotrophin-dependent synaptic plasticity by deletion of glial aquaporin-4. J Neurosci 2011; 31(17): 6392-7.
  26. Shah NR, Braverman ER. Measuring adiposity in patients: the utility of body mass index (BMI), percent body fat, and leptin. PLoS One 2012; 7(4): e33308.
  27. Miller AA, Spencer SJ. Obesity and neuroinflammation: A pathway to cognitive impairment. Brain Behav Immun 2014; 42: 10-21.
  28. Cournot M, Marquie JC, Ansiau D, Martinaud C, Fonds H, Ferrieres J, et al. Relation between body mass index and cognitive function in healthy middle-aged men and women. Neurology 2006; 67(7): 1208-14.
  29. Sabia S, Kivimaki M, Shipley MJ, Marmot MG, Singh-Manoux A. Body mass index over the adult life course and cognition in late midlife: The Whitehall II Cohort Study. Am J Clin Nutr 2009; 89(2): 601-7.
  30. Elias MF, Elias PK, Sullivan LM, Wolf PA, D'Agostino RB. Lower cognitive function in the presence of obesity and hypertension: The Framingham heart study. Int J Obes Relat Metab Disord 2003; 27(2): 260-8.
  31. Dye L, Boyle NB, Champ C, Lawton C. The relationship between obesity and cognitive health and decline. Proc Nutr Soc 2017; 76(4): 443-54.
  32. Min JH, Waters P, Vincent A, Cho HJ, Joo BE, Woo SY, et al. Low levels of vitamin D in neuromyelitis optica spectrum disorder: Association with disease disability. PLoS One 2014; 9(9): e107274.
  33. Eskandarieh S, Nedjat S, Abdollahpour I, Azimi AR, Moghadasi AN, Asgari N, et al. Environmental risk factors in neuromyelitis optica spectrum disorder: A case-control study. Acta Neurol Belg 2018; 118(2): 277-87.
  34. Gregor MF, Hotamisligil GS. Inflammatory mechanisms in obesity. Annu Rev Immunol 2011; 29: 415-45.
  35. Spencer SJ. Perinatal nutrition programs neuroimmune function long-term: mechanisms and implications. Front Neurosci 2013; 7: 144.
  36. Koessler S, Engler H, Riether C, Kissler J. No retrieval-induced forgetting under stress. Psychol Sci 2009; 20(11): 1356-63.