Evaluation of Patients with Multiple Sclerosis in Terms of Memory, Attention, Executive Functions, Fine Motor Movement and the Association thereof with Magnetic Resonance Imaging Results

Abstract

Aim: This study aimed to review cognitive function and fine motor skills in patients with multiple sclerosis (MS) and investigate the association with magnetic resonance imaging (MRI) results. Material and Methods: The study included 22 patients diagnosed with relapsing-remitting MS and 22 controls. Participants underwent neuropsychological tests, including the Stroop test, Rey auditory verbal learning test (RAVLT), line bisection test (LBT), serial reaction time test (SRTT), and finger tapping test (FTT). The relationship between severity of disease, MRI, and test performance was investigated. Results: It was determined that the patients were lateralized to the right in the LBT data, while the control group was lateralized to the left (p=0.024). On cognitive tests, there was no significant difference in Stroop test results (p=0.134), but the mean overall RAVLT of the patient group was significantly lower than that of the control group (p<0.001). Patients had significantly longer reaction times in SRTT (p=0.038). A positive correlation was found between the expanded disability status scale (EDSS) score and LBT results (r=0.326, p=0.031), and a negative correlation between RAVLT results and EDSS score. For fine motor skills, a negative correlation was observed between FTT results and the number of MS plaques in the left hemisphere (r=-0.431, p=0.045), and a positive correlation between the number of SRTT error and the number of plaques in the juxtacortical regions (r=0.461, p=0.031). Conclusion: This study shows that the impairment of cognitive functions in MS disease is associated with both the course and severity of the disease and MRI findings.

Keywords

• Multiple Sclerosis
• Cognitive Functions
• Neuroanatomical Localization
• Fine Motor Skills

Multiple Sklerozlu Hastaların Bellek, Dikkat, Yürütücü İşlevler, İnce Motor Hareket Yönünden Değerlendirilmesi ve Bunların Manyetik Rezonans Görüntüleme Bulguları ile İlişkisi

Abstract

Amaç: Bu çalışmada multipl skleroz (MS) hastalarının bilişsel işlevleri ve ince motor becerilerinin gözden geçirilmesi ve bunların manyetik rezonans görüntüleme (MRG) sonuçları ile ilişkisinin araştırılması amaçlandı. Gereç ve Yöntemler: Çalışmaya relaps-remisyon tipi MS tanısı alan 22 hasta ve 22 kontrol grubu dahil edildi. Katılımcılara Stroop testi, Rey işitsel sözel öğrenme testi (Rey auditory verbal learning test, RAVLT), çizgi bölme testi (ÇBT), seri seçim reaksiyon testi (SSRT) ve parmak vuru testi (PVT) dahil olmak üzere nöropsikolojik testler uygulandı. Hastalık şiddeti ve MRG ile test performansı arasındaki ilişki de incelendi. Bulgular: Elde edilen sonuçlara göre ÇBT verilerinde hastaların sağa lateralize olduğu, kontrol grubunun ise sola lateralize olduğu tespit edildi (p=0,024). Bilişsel testlerde, Stroop testi sonuçları arasında anlamlı bir fark bulunmazken (p=0,134), hasta grubunun genel RAVLT ortalaması kontrol grubuna göre anlamlı derecede düşüktü (p<0,001). Hastaların SRTT’deki ortalama reaksiyon süresi anlamlı derecede daha uzundu (p=0,038). Genişletilmiş engellilik durumu ölçeği (expanded disability status scale, EDSS) skoru ile ÇBT sonuçları arasında pozitif bir korelasyon (r=0,326; p=0,031) ve RAVLT sonuçları ile EDSS skoru arasında negatif bir korelasyon belirlendi. İnce motor becerilerde, sağ el PVT sonuçları ile sol hemisferdeki MS plağı sayısı arasında negatif bir korelasyon (r=-0,431; p=0,045) ve SSRT hata sayısı ile jukstakortikal bölgelerdeki plak sayısı arasında pozitif bir korelasyon (p=0.031) tespit edildi. Sonuç: Bu çalışma, MS hastalığında bilişsel işlevlerdeki bozulmanın hem hastalığın seyri ve şiddetiyle hem de MR bulgularıyla ilişkili olduğunu göstermiştir.

Keywords

• Multipl Skleroz
• Bilişsel İşlevler
• Nöroanatomik Lokalizasyon
• İnce Motor Beceri

References

1. Ropper AH, Samuels MA. Adams and Victor’s principles of neurology. 9th ed. Translated by Emre M. Ankara: Güneş Medical Publishing House; 2011. p.874-903. Turkish.
2. Altıntaş A. Immunopathogenesis and pathology of multiple sclerosis. Turkiye Klinikleri J Neurol-Special Topics. 2009;2(2):1-8. Turkish.
3. Randall TS. Managing the symptoms of multiple sclerosis. 4th ed. New York: Demos Medical Publishing; 2006.
4. Mitchell AJ, Benito-Leon J, Gonzalez JM, Rivera-Navarro J. Quality of life and its assessment in multiple sclerosis: integrating physical and psychological components of wellbeing. Lancet Neurol. 2005;4(9):556-66.
5. Langdon DW. Cognition in multiple sclerosis. Curr Opin Neurol. 2011;24(3):244-9.
6. Morrow SA, Weinstock-Guttman B, Munschauer F, Hojnacki D, Benedict RHB. Subjective fatigue is not associated with cognitive impairment in multiple sclerosis: cross-sectional and longitudinal analysis. Mult Scler. 2009;15(8):998-1005.
7. Chiaravalloti ND, DeLuca J. Cognitive impairment in multiple sclerosis. Lancet Neurol. 2008;7(12):1139-51.
8. Longstaff MG, Heath RA. Spiral drawing performance as an indicator of fine motor function in people with multiple sclerosis. Hum Mov Sci. 2006;25(4-5):474-91.

9. Shirani A, Newton BD, Okuda DT. Finger tapping impairments are highly sensitive for evaluating upper motor neuron lesions. BMC Neurol. 2017;17(1):55.
10. Goverover Y, Sandroff BM, DeLuca J. Dual task of fine motor skill and problem solving in individuals with multiple sclerosis: a pilot study. Arch Phys Med Rehabil. 2018;99(4):635-40.
11. Squillace M, Ray S, Milazzo M. Changes in gross grasp strength and fine motor skills in adolescents with pediatric multiple sclerosis. Occup Ther Health Care. 2015;29(1):77-85.
12. Roelofs A. Goal-referenced selection of verbal action: modeling attentional control in the Stroop task. Psychol Rev. 2003;110(1):88-125.
13. Rosenberg SJ, Ryan JJ, Prifitera A. Rey Auditory-Verbal Learning Test performance of patients with and without memory impairment. J Clin Psychol. 1984;40(3):785-7.
14. Güneş E, Nalçacı E, Kalaycıoğlu C, Çiçek M, Kara F. Line bisection task and test-retest reliability. J Psychiatry Psychol Psychopharmacol (3P). 2002;10(1):33-40. Turkish.
15. Nalçacı E, Çiçek M, Kalaycıoğlu C. Quantitative EEG analysis during the line bisection test. SBAG-1884, Ankara: TÜBİTAK; 2000. Turkish.
16. Robertson EM. The serial reaction time task: implicit motor skill learning. J Neurosci. 2007;27(38):10073-5.
17. Giovannoni G, van Schalkwyk J, Fritz VU, Lees AJ. Bradykinesia akinesia incoordination test (BRAIN TEST): an objective computerised assessment of upper limb motor function. J Neurol Neurosurg Psychiatry. 1999;67(5):624-9.
18. Bodling AM, Denney DR, Lynch SG. Individual variability in speed of information processing: an index of cognitive impairment in multiple sclerosis. Neuropsychology. 2012;26(3):357-67.
19. Hughes AJ, Denney DR, Lynch SG. Reaction time and rapid serial processing measures of information processing speed in multiple sclerosis: complexity, compounding, and augmentation. J Int Neuropsychol Soc. 2011;17(6):1113-21.
20. Denney DR, Gallagher KS, Lynch SG. Deficits in processing speed in patients with multiple sclerosis: evidence from explicit and covert measures. Arch Clin Neuropsychol. 2011;26(2):110-9.
21. Covey TJ, Golan D, Doniger GM, Sergott R, Zarif M, Srinivasan J, et al. Visual evoked potential latency predicts cognitive function in people with multiple sclerosis. J Neurol. 2021;268(11):4311-20.
22. Barlow-Krelina E, Fabri TL, O’Mahony J, Gur RC, Gur RE, De Somma E, et al. Examining cognitive speed and accuracy dysfunction in youth and young adults with pediatric-onset multiple sclerosis using a computerized neurocognitive battery. Neuropsychology. 2021;35(4):388-98.
23. Thornton AE, Raz N, Tucker KA. Memory in multiple sclerosis: contextual encoding deficits. J Int Neuropsychol Soc. 2002;8(3):395-409.
24. Scherer P, Penner IK, Rohr A, Boldt H, Ringel I, Wilke-Burger H, et al. The faces symbol test, a newly developed screening instrument to assess cognitive decline related to multiple sclerosis: first results of the Berlin Multi-Centre FST Validation Study. Mult Scler. 2007;13(3):402-11.
25. Cerezo Garcia M, Martín Plasencia P, Aladro Benito Y, Balseiro Gómez JJ, Rueda Marcos A. Executive function and memory in patients with relapsing-remitting multiple sclerosis. Psicothema. 2009;21(3):416-20.
26. Schulz D, Kopp B, Kunkel A, Faiss JH. Cognition in the early stage of multiple sclerosis. J Neurol. 2006;253(8):1002-10.
27. Gaudino EA, Chiaravalloti ND, DeLuca J, Diamond BJ. A comparison of memory performance in relapsing-remitting, primary progressive and secondary progressive, multiple sclerosis. Neuropsychiatry Neuropsychol Behav Neurol. 2001;14(1):32-44.
28. Demers M, Rouleau I, Scherzer P, Ouellet J, Jobin C, Duquette P. Impact of the cognitive status on the memory complaints in MS patients. Can J Neurol Sci. 2011;38(5):728-33.
29. Kenealy PM, Beaumont JG, Lintern TC, Murrell RC. Autobiographical memory in advanced multiple sclerosis: assessment of episodic and personal semantic memory across three time spans. J Int Neuropsychol Soc. 2002;8(6):855-60.
30. Miyazaki Y, Niino M, Takahashi E, Nomura T, Naganuma R, Amino I, et al. Stages of brain volume loss and performance in the Brief International Cognitive Assessment for Multiple Sclerosis. Mult Scler Relat Disord. 2022;67:104183.
31. Hoffmann JA, Bareuther L, Schmidt R, Dettmers C. The relation between memory and decision-making in multiple sclerosis patients. Mult Scler Relat Disord. 2020;37:101433.
32. Sehanovic A, Kunic S, Ibrahimagic OC, Smajlovic D, Tupkovic E, Mehicevic A, et al. Contributing factors to the quality of life in multiple sclerosis. Med Arch. 2020;74(5):368-73.
33. Rogers JM, Panegyres PK. Cognitive impairment in multiple sclerosis: Evidence-based analysis and recommendations. J Clin Neurosci. 2007;14(10):919-27.
34. Hechtman L, McGough JJ. Attention-Deficit Disorders. In: Kaplan & Sadock’s comprehensive textbook of psychiatry. 8th ed. Translated by Öner Ö, Aysev A. Aydın H, Bozkurt A, editors. Ankara: Güneş Medical Publishing House; 2007. p.3183-205. Turkish.
35. Doyle BB. Understanding and treating adults with attention deficit hyperactivity disorder. 1st ed. Washington: American Psychiatric Pub; 2006. p.1-31.
36. De Sonneville LM, Boringa JB, Reuling IEW, Lazeron RHC, Ader HJ, Polman CH. Information processing characteristics in subtypes of multiple sclerosis. Neuropsychologia. 2002;40(11):1751-65.
37. Öktem Ö. Neuropsychological tests and neuropsychological assessment. Turk J Psychol. 1994;9(33):33-44. Turkish.
38. Kocsis K, Szabó N, Tóth E, Király A, Faragó P, Kincses B, et al. The effect of lesion location on visuospatial attentional bias in patients with multiple sclerosis. Neuropsychology. 2022;36(2):150-8.
39. Gilad R, Sadeh M, Boaz M, Lampl Y. Visual spatial neglect in multiple sclerosis. Cortex. 2006;42(8):1138-42.
40. Gerloff C, Corwell B, Chen R, Hallett M, Cohen LG. The role of the human motor cortex in the control of complex and simple finger movement sequences. Brain. 1998;121(Pt 9):1695-709.