Information Processing Speed Assessed with Letter Digit Substitution Test in Croatian Sample of Multiple Sclerosis Patients

Ana Jerković, Meri Matijaca, Ana Proroković, Anđela Šikić, Vana Košta, Ana Ćurković Katić, Krešimir Dolić, Klaudia Duka Glavor, Joško Šoda, Zoran Đogaš, Maja Rogić Vidaković, Ana Jerković, Meri Matijaca, Ana Proroković, Anđela Šikić, Vana Košta, Ana Ćurković Katić, Krešimir Dolić, Klaudia Duka Glavor, Joško Šoda, Zoran Đogaš, Maja Rogić Vidaković

Abstract

Cognitive impairment is a common complaint in people with multiple sclerosis (pwMS). The study objective was to determine the psychometric properties of the letter digit substitution test (LDST) that measures information processing speed and to investigate the impact of relevant predictors of LDST achievement in pwMS. The design was cross-sectional. The study included 87 pwMS and 154 control subjects. The validity of LDST was examined, and a hierarchical regression model was used to explore relevant predictors of LDST success. The LDST had excellent construct validity, as expressed by differences between pwMS and control subjects. Convergent validity of the LDST was supported by a significant moderate correlation with the expanded disability status scale (EDSS) (ρ = -0.36; p < 0.05) and a significantly strong correlation with the multiple sclerosis impact scale (MSIS-29) physical subscale (r = -0.64; p < 0.01). The LDTS score well differentiated the pwMS considering age, education, EDSS, disease duration, comorbidity, and medication therapy. Using the LDST as a criterion variable in pwMS results showed consistent evidence for the age, education, and EDSS impact on LDST performance. The best cut-off score of ≤35 discriminated the control and MS group. LDST proved to be a valid test for assessing information processing speed in pwMS.

Keywords: Letter Digit Substitution Test; cognition; cognitive measure; information processing speed; multiple sclerosis.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Box plots showing means and standard deviations of LDST in pwMS and control subjects.
Figure 2
Figure 2
Changes in LDST performance regarding age, education, EDSS, duration of disease, comorbidity, and immunomodulatory drug use in pwMS.
Figure 3
Figure 3
ROC curve of LDST.

References

    1. Howard J., Trevick S., Younger D.S. Epidemiology of Multiple Sclerosis. Neurol. Clin. 2016;34:919–939. doi: 10.1016/j.ncl.2016.06.016.
    1. Chiaravalloti N.D., DeLuca J. Cognitive impairment in multiple sclerosis. Lancet Neurol. 2008;7:1139–1151. doi: 10.1016/S1474-4422(08)70259-X.
    1. Guimarães J., Sá M.J. Cognitive dysfunction in multiple sclerosis. Front. Neurol. 2012;3:74. doi: 10.3389/fneur.2012.00074.
    1. Van Schependom J., D‘hooghe M.B., Cleynhens K., D’hooge M., Haelewyck M.C., De Keyser J., Nagels G. Reduced information processing speed as primum movens for cognitive decline in MS. Mult. Scler. 2015;21:83–91. doi: 10.1177/1352458514537012.
    1. Smith A. Symbol Digit Modalities Test: Manual. Western Psychological Services; Los Angeles, CA, USA: 1982.
    1. Van der Elst W., Van Boxtel M.P., Van Breukelen G.J., Jolles J. The Letter Digit Substitution Test: Normative data for 1858 healthy participants aged 24–81 from the Maastricht Aging Study (MAAS): Influence of age, education, and sex. J. Clin. Exp. Neuropsychol. 2006;28:998–1009. doi: 10.1080/13803390591004428.
    1. Jolles J., van Boxtel M.P., Ponds R.W., Metsemakers J.F., Houx P.J. The Maastricht aging study (MAAS). The longitudinal perspective of cognitive aging. Tijdschr. Gerontol. Geriatr. 1998;29:120–129.
    1. Wechsler D. Manual for the Wechsler Adult Intelligence Scale-Revised. Psychological Corporation; New York, NY, USA: 1981.
    1. Langdon D.W., Amato M.P., Boringa J., Brochet B., Foley F., Fredrikson S., Hamalainen P., Hartung H.P., Krupp L., Penner I.K. Recommendations for a Brief International Cognitive Assessment for Multiple Sclerosis (BICAMS) Mult. Scler. 2012;18:891–898. doi: 10.1177/1352458511431076.
    1. Hobart J., Lamping D., Fitzpatrick R., Riazi A., Thompson A. The Multiple Sclerosis Impact Scale (MSIS-29); a new patient-based outcome measure. Brain. 2001;124:962–973. doi: 10.1093/brain/124.5.962.
    1. Rogić Vidaković M., Šimić N., Poljičanin A., Ivanišević M.N., Ana J., Đogaš Z. Psychometric properties of the Croatian Version of the Depression, Anxiety, and Stress Scale-21 and Multiple Sclerosis Impact Scale-29 in Multiple Sclerosis Patients. Mult. Scler. Relat. Disord. 2021;50:102850. doi: 10.1016/j.msard.2021.102850.
    1. Lublin F.D., Reingold S.C., Cohen J.A., Cutter G.R., Sorensen P.S., Thompson A.J., Wolinsky J.S., Balcer L.J., Banwell B., Barkhof F., et al. Defining the clinical course of multiple sclerosis: The 2013 revisions. Neurology. 2014;83:278–286. doi: 10.1212/WNL.0000000000000560.
    1. Kurtzke J.F. Rating neurologic impairment in multiple sclerosis: An expanded disability status scale (EDSS) Neurology. 1983;33:1444–14452. doi: 10.1212/WNL.33.11.1444.
    1. Møller J.T., Cluitmans P., Rasmussen L.S., Houx P., Rasmussen H., Canet J., Rabbitt P., Jolles J., Larsen K., Hanning C.D., et al. Long-term postoperative cognitive dysfunction in the elderly: ISPOCD1 study. Lancet. 1998;351:857–861. doi: 10.1016/S0140-6736(97)07382-0.
    1. De Groot R.H.M., Hornstra G., Rozendaal N., Jolles J. Memory performance, but not information processing speed, may be reduced during early pregnancy. J. Clin. Exp. Neuropsychol. 2003;25:482–488. doi: 10.1076/jcen.25.4.482.13871.
    1. Dijkstra J.B., Strik J.J.M.H., Lousberg R., Prickaerts J., Riedel W.J., Jolles J., van Praag H.M., Honig A. Atypical cognitive profile in patients with depression after myocardial infarction. J. Affect. Disord. 2002;70:181–190. doi: 10.1016/S0165-0327(01)00348-2.
    1. Jelicic M., Van Boxtel M.P.J., Houx P.J., Jolles J. Does migraine headache affect cognitive function in the elderly? Report from the Maastricht Aging Study (MAAS) Headache. 2000;40:715–719. doi: 10.1046/j.1526-4610.2000.00124.x.
    1. Van Boxtel P.J., Gaillard C., Houx P.J., Buntinx F., de Leeuw P.W., Jolles J. Can blood pressure predict cognitive task performance in a healthy population sample? J. Hypertens. 1997;15:1069–1076. doi: 10.1097/00004872-199715100-00004.
    1. Knežević M., Tarabić B.N., Tomac P., Vincek A., Ivanda L. Uloga dobi, spola i obrazovanja u brzini procesiranja informacija [Role of age, gender and education in information processing speed] Psihologijske Teme. 2015;24:173–185.
    1. Benedict RHb DeLuca J., Phillips G., LaRocca N., Hudson L.D., Rudick R., Multiple Sclerosis Outcome Assessments Consortium Validity of the Symbol Digit Modalities Test as a cognition performance outcome measure for multiple sclerosis. Mult. Scler. 2017;23:721–733. doi: 10.1177/1352458517690821.
    1. Brochet B., Ruet A. Cognitive Impairment in Multiple Sclerosis with Regards to Disease Duration and Clinical Phenotypes. Front. Neurol. 2019;10:261. doi: 10.3389/fneur.2019.00261.
    1. Rooney S., Wood L., Moffat F., Paul L. Prevalence of fatigue and its association with clinical features in progressive and non-progressive forms of Multiple Sclerosis. Mult. Scler. Relat. Disord. 2019;28:276–282. doi: 10.1016/j.msard.2019.01.011.
    1. Polman C.H., Reingold S.C., Edan G., Filippi M., Hartung H.-P., Kappos L., Lublin F.D., Metz L.M., McFarland H.F., O’Connor P.W. Diagnostic criteria for multiple sclerosis: 2005 revisions to the “McDonald criteria”. Ann. Neurol. 2005;58:840–846. doi: 10.1002/ana.20703.
    1. Katz Sand I. Classification, diagnosis, and differential diagnosis of multiple sclerosis. Curr. Opin. Neurol. 2015;28:193–205. doi: 10.1097/WCO.0000000000000206.
    1. Dusankova J.B., Kalincik T., Havrdova E., Benedict R.H. Cross cultural validation of the Minimal Assessment of Cognitive Function in Multiple Sclerosis (MACFIMS) and the Brief International Cognitive Assessment for Multiple Sclerosis (BICAMS) Clin. Neuropsychol. 2012;26:1186–1200. doi: 10.1080/13854046.2012.725101.
    1. Filser M., Schreiber H., Pöttgen J., Ullrich S., Lang M., Penner I.K. The Brief International Cognitive Assessment in Multiple Sclerosis (BICAMS): Results from the German Validation Study. J. Neurol. 2018;265:2587–2593. doi: 10.1007/s00415-018-9034-1.
    1. Goretti B., Niccolai C., Hakiki B., Sturchio A., Falautano M., Minacapelli E., Martinelli V., Incerti C., Nocentini U., Murgia M., et al. The Brief International Cognitive Assessment for Multiple Sclerosis (BICAMS): Normative values with gender, age and education corrections in the Italian population. BMC Neurol. 2014;14:171. doi: 10.1186/s12883-014-0171-6.
    1. Marstrand L., Østerberg O., Walsted T., Skov A.C., Schreiber K.I., Sellebjerg F. Brief international cognitive assessment for multiple sclerosis (BICAMS): A danish validation study of sensitivity in early stages of MS. Mult. Scler. Relat. Disord. 2020;37:101458. doi: 10.1016/j.msard.2019.101458.
    1. Estiasari R., Fajrina Y., Lastri D.N., Melani S., Maharani K., Imran D., Pangeran D., Sitorus F. Validity and Reliability of Brief International Cognitive Assessment for Multiple Sclerosis (BICAMS) in Indonesia and the Correlation with Quality of Life. Neurol. Res. Int. 2019;2019:4290352. doi: 10.1155/2019/4290352.
    1. Sandi D., Rudisch T., Füvesi J., Fricska-Nagy Z., Huszka H., Biernacki T., Langdon D.W., Langane E., Vecsei L., Bencsik K. The Hungarian validation of the Brief International Cognitive Assessment for Multiple Sclerosis (BICAMS) battery and the correlation of cognitive impairment with fatigue and quality of life. Mult. Scler. Relat. Disord. 2015;4:499–504. doi: 10.1016/j.msard.2015.07.006.
    1. Sousa C., Rigueiro-Neves M., Miranda T., Alegria P., Vale J., Passos A.M., Langdon D., Sá M.J. alidation of the brief international cognitive assessment for multiple sclerosis (BICAMS) in the Portuguese population with multiple sclerosis. BMC Neurol. 2018;18:172. doi: 10.1186/s12883-018-1175-4.
    1. Betscher E., Guenter W., Langdon D.W., Bonek R. Polish validation of the Brief International Cognitive Assessment for Multiple Sclerosis (BICAMS battery): Correlation of cognitive impairment with mood disorders and fatigue. Neurol. Neurochir. Pol. 2021;55:59–66. doi: 10.5603/PJNNS.a2020.0080.
    1. Alarcón A.N., Ayala O.D., García J.R., Montaňés P. Validation of the Brief International Cognitive Assessment for Multiple Sclerosis (BICAMS) in a Colombian Population. Mult. Scler. Relat. Disord. 2020;42:102072. doi: 10.1016/j.msard.2020.102072.
    1. Hämäläinen P., Leo V., Therman S., Ruutiainen J. Validation of the Finnish version of the Brief International Cognitive Assessment for Multiple Sclerosis (BICAMS) and evaluation of the applicability of the Multiple Sclerosis Neuropsychological Questionnaire (MSNQ) and the Fatigue Scale for Motor and Cognitive Functions (FSMC) Brain Behav. 2021;11:e02087.
    1. Polychroniadou E., Bakirtzis C., Langdon D., Lagoudaki R., Kesidou E., Theotokis P., Tsalikakis D., Poulatsidou K., Kyriazis O., Boziki M., et al. Validation of the Brief International Cognitive Assessment for Multiple Sclerosis (BICAMS) in Greek population with multiple sclerosis. Mult. Scler. Relat. Disord. 2016;9:68–72. doi: 10.1016/j.msard.2016.06.011.
    1. Niino M., Fukazawa T., Kira J.I., Okuno T., Mori M., Sanjo N., Ohashi T., Fukaura H., Fujimori J., Shimizu Y., et al. Validation of the Brief International Cognitive Assessment for Multiple Sclerosis in Japan. Mult. Scler. J. Exp. Transl. Clin. 2017;3:2055217317748972. doi: 10.1177/2055217317748972.
    1. Maubeuge N., Deloire M.S.A., Brochet B., Erhlé N., Charré-Morin J., Saubusse A., Ruet A., BICAFMS Study Investigators French validation of the Brief International Cognitive Assessment for Multiple Sclerosis. Rev. Neurol. 2021;177:73–79. doi: 10.1016/j.neurol.2020.04.028.

Source: PubMed

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