See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/321020554

Reliability of BICAMS (Arabic version) in Egyptian multiple sclerosis patients

Article  in  Multiple Sclerosis · October 2017

CITATIONS READS

4 395

11 authors, including:

Nirmeen Kishk Nevin Shalaby

Cairo University,school of medicine Cairo University
85 PUBLICATIONS   386 CITATIONS    84 PUBLICATIONS   295 CITATIONS   

SEE PROFILE SEE PROFILE

hatem shehata Amr Hassan

Cairo University Cairo University
106 PUBLICATIONS   392 CITATIONS    58 PUBLICATIONS   188 CITATIONS   

SEE PROFILE SEE PROFILE

Some of the authors of this publication are also working on these related projects:

Egyptian people,protection against hepatitis c and Covid-19 View project

LDN, COVID-19 View project

All content following this page was uploaded by Nevin Shalaby on 05 August 2021.

The user has requested enhancement of the downloaded file.

Farghaly et al. The Egyptian Journal of Neurology, Psychiatry and Neurosurgery
(2021) 57:51
The Egyptian Journal of Neurology,
https://doi.org/10.1186/s41983-021-00303-6 Psychiatry and Neurosurgery

RESEARCH Open Access

Reliability and validity of Arabic version of

the brief international cognitive assessment
for multiple sclerosis: Egyptian dialect
Marwa Farghaly1, Dawn W. Langdon2, Nevin M. Shalaby1* , Hatem S. Shehata1, Noha T. Abokrysha1, Amr Hassan1,
Mohamed I. Hegazy1, Alaa Elmazny1, Sandra Ahmed1, Shaimaa Shaheen1, Alshaimaa S. Othman1,
Osama Yacoub1 and Nirmeen A. Kishk1

Abstract
Background: Given the diversity of multiple sclerosis (MS) symptoms including cognitive impairment in certain
domains, the need to develop a rapid and at the same time thorough tool for cognitive assessment is mandatory
and represents an unmet need in the clinical and research fields of MS. The Brief International Cognitive
Assessment for MS (BICAMS) is a good and practical tool to achieve this mission but is not present in the Arabic
language for Arabic speaking countries yet.
Objectives: To assess the reliability and validity of Arabic version of the BICAMS (Egyptian dialect).
Methods: Ninety Egyptian MS patients and 85 matched healthy controls underwent neuropsychological testing
using the BICAMS Arabic version (Egyptian dialect) battery including the Symbol Digit Modality Test (SDMT),
California Verbal Learning Test 2nd edition (CVLT-II), and revised Brief Visuospatial Retention Test- (BVRT-R). Test–
retest data were obtained from MS patients 2 weeks after the initial assessment. Mean differences between both
groups were assessed controlling for age, gender, and educational level.
Results: The MS patients scored significantly lower on the SDMT, CVLT-II, and BVMT-R tests compared to healthy
controls (p<0.001). For MS patients’ group, intra-observer (test–retest) reliability was satisfactory for SDMT, CVLT-II
total, and BVRT-R total with r values of 0.85, 0.61, and 0.68, respectively.
Conclusion: BICAMS Arabic version is a reliable and valid tool for cognitive assessment of Arabic speaking MS
patients in different clinical and research settings.
Keywords: BICAMS, Arabic version, Multiple sclerosis, Cognitive assessment, Reliability, Validity

Introduction to manage factors that increase disability such as cogni-

Multiple sclerosis (MS) is a common neurological dis- tive impairment is crucial. The burden of MS on the
ease which causes physical, psychological, and cognitive patients’ cognitive function [4] is well established; MS
disabilities. MS is associated with high rates of un- patients show greater impairments on tests of non-
employment in Egypt [1], the prevalence of MS in Egypt verbal intellectual ability, processing speed, and select-
has been shown to be 13.7/100,000 and 25/100,000 in ive/focused attention, verbal-recall, and verbal fluency
two studies, respectively [2, 3], and so early assessment skills [5, 6]. Assessment of cognition in MS started late
in the 1980s when Rao and colleagues started addressing
* Correspondence: [email protected]
information processing speed slowing in patients with
1
Neurology department, Kasr Al-Ainy School of Medicine, Al-Saraya St, MS. [7] Consequently, several cognitive batteries for MS
Al-Manial district, Cairo, Egypt patients were developed as “Brief Repeatable Battery
Full list of author information is available at the end of the article

© The Author(s). 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License,
which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give
appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if
changes were made. The images or other third party material in this article are included in the article's Creative Commons
licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons
licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain
permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
Farghaly et al. The Egyptian Journal of Neurology, Psychiatry and Neurosurgery (2021) 57:51 Page 2 of 8

(BRB) of Neuropsychological Tests,” [8] “MS Functional placed in the hospital calling for volunteers to partici-
Composite” (MSFC), [4] “Minimal Assessment of Cogni- pate in a study directed to cognitive assessment. Partici-
tive Function in MS” (MACFIMS), [9] “MS-Cog,” [10] pants included paramedical staff, caregivers, and
and the National Institute of Neurological Disorders and patients’ relatives (first-degree relatives were excluded).
Stroke (NINDS) has a series of recommended assess- Volunteers with history of drug abuse or history of psy-
ments across multiple clinical domains for several chiatric disease or medication that interferes with cogni-
neurological diseases, called “Common Data Elements” tion were excluded.
(CDE) and MS standards [11]. Most recently, the “Brief The test was performed by the clinical staff in Kasr
International Cognitive Assessment for MS” (BICAMS) Al-Ainy MS clinic; all clinical staff participating in this
has been recommended [12, 13]. BICAMS is a validated study attended a training session to ensure unified ad-
test for detection of cognitive impairment in MS patients ministration procedures and data recording. The scoring
that can be completed by a neurologist. Symbol Digit of the test for all participants was performed by the
Modalities Test (SDMT), [14] the five initial learning same researcher. All participants provided informed
trials of the second edition of the California Verbal written consent to all procedures. The study was ap-
Learning Test (CVLT-II), [15] and the revised Brief proved by the neurology ethical scientific committee,
Visuospatial retention Test (BVRT-R) [16] are well neurology department, Cairo University, February 2017.
established psychometric tests and are of documented This committee does not provide a reference number.
good face validity and consistent stimulus presentation. BICAMS was performed for all patients in the
The Egyptian Arabic dialect is the most recognized morning in a quiet room during patient’s scheduled
and widely understood dialect by Arabic speakers regular visits; it included three tests: Symbol Digit
around the world. Although there are several neuro- Modalities Test (SDMT), the California Verbal Learn-
psychological tests in classical Arabic language, lack of ing Test (CVLT-II), and the revised Brief Visuospatial
Arabic tests for MS matching Egyptian culture and dia- retention Test (BVRT-R). The tests were administered
lect is an obstacle in neuropsychological assessment of in the same sequence: SDMT, CVLT-II, first 5 trials,
patients in Egypt. In this study, our objective was to as- and BVRT-R, first 3 recall trials. We followed the
sess the reliability and validity of the Arabic translation suggested international validation standards of
of the BICAMS test. BICAMS [13].

Methods
Patients were recruited from Kasr Al-Ainy MS clinic in Step (1): Standardization and Translation of Test Stimuli
Cairo University consecutively between March and July BICAMS was translated and culturally adapted into
2017. Around 817 patients with MS diagnosis based on the Arabic language. The SDMT (oral) [18] presents a
the revised McDonald’s criteria [17] visited the MS clinic series of nine symbols, and each paired with a single
during this period either for regular follow-up visits or digit in a key at the top of a standard sheet of paper.
in an attack, only patients fulfilling inclusion criteria An adapted version of the test is used and numbers
were recruited. The inclusion criteria were patients 18– used for instructions and response were in the Arabic
55 years of age, with no evidence of relapse or steroids language. Participants were asked to say the digit
intake during the previous 4 weeks before enrollment. associated with each symbol as rapidly as possible for
Patients were excluded if they were illiterate, or had a 90 s. The number of correct responses in 90 s was
history of any neuropsychiatric disorder other than MS, recorded. The CVLT-II [15]: the CVLT-II list of
a history of drug abuse or cognitive enhancing medica- words was translated and retranslated from English to
tion, or having systemic diseases or metabolic disorders Arabic by a professional translator. Four semantic
that may impair cognition, any visual, or hearing prob- categories were used: cooking utensils, vegetables,
lem that could interfere with performance of the test, or clothes, and tools. Cooking utensils were chosen be-
EDSS ≥7, as well as those residing in governates other cause this matches Egyptian culture familiarity more
than Great Cairo (as they may not be able to come back than different types of sports. Words of average famil-
in the retesting step). All patients participated voluntar- iarity and frequency in Egypt culture were used
ily. Age, gender, years of education, MS subtype, age of (Table 1). The total number of recalled items over
onset, Expanded Disability Status Scale (EDSS), and dis- the five learning trials was calculated (CVLT TL). Vis-
ease duration were recorded. Figure 1 shows the flow- ual/spatial memory is assessed in BICAMS using the
chart of patients’ recruitment. BVRT-R [16], and for visual stimuli, six abstract de-
Ninety patients were recruited and compared with 85 signs that have no semantic associations to stimuli in
healthy participants in the control group. The healthy the culture or language in Egypt were used. The total
control (HC) group was recruited by an advertisement score of the three trials was calculated (BVRT TL).
Farghaly et al. The Egyptian Journal of Neurology, Psychiatry and Neurosurgery (2021) 57:51 Page 3 of 8

Fig. 1 Flowchart showing the recruitment process of patients with multiple sclerosis for the study

Step (2): Standardization and Translation of Test reliability. All tests and procedures were identical to the
Instructions first visit with the same examiner, and all retests were
All information from the test manual necessary for ad- scored with the same rater who scored the first visit test.
ministration and interpretation was translated, back Only intra-rater assessment was carried out without
translated, and checked for errors in Arabic language inter-rater comparisons as this was the discipline
(Egyptian Dialect). All examiners were trained to use adopted by the international group of BICAMS.
standardized instructions in Arabic language.
Step (4): Criterion-related validity
Step (3): Test–retest reliability The MS sample was compared to a healthy control
Forty-eight MS patients and 44 healthy volunteers were group to determine if BICAMS is sensitive to MS disease
assessed on two occasions separated by 2 weeks to test state. Impairment on individual tests was defined as −1.5
standard deviation (SD) below reference group means.
Table 1 Standardization of California Verbal Learning Test using
Data was coded and entered using the IBM statistical
familiar and frequent words in Egyptian culture package SPSS (Statistical Package for the Social
‫ ﺟﺎﻛﻴﺖ‬/ ‫ﺟﺰﺭ‬
Sciences) for windows, version 24, released 2016,
Armonk, New York. Data was summarized using mean,
‫ ﺣﻠﺔ‬/‫ﺷﺎﻛﻮﺵ‬
standard deviation, median, minimum, and maximum in
‫ ﺑﻨﻄﻠﻮﻥ‬/‫ﻣﺴﻤﺎﺭ‬ quantitative data and using frequency (count) and
‫ ﻣﺼﻔﺎﺓ‬/‫ﺧﺲ‬ relative frequency (percentage) for categorical data.
‫ ﻣﻐﺮﻓﺔ‬/‫ﺟﺰﻣﺔ‬ Comparisons between quantitative variables were done
‫ ﻣﻨﺸﺎﺭ‬/ ‫ﻗﻤﺢ‬ using the non-parametric Kruskal-Wallis and Mann-
‫ ﻓﺴﺘﺎﻥ‬/ ‫ﻃﺎﺳﺔ‬
Whitney tests. For comparison of serial measurements
within each patient, the non-parametric Wilcoxon
‫ ﻛﻮﺳﺔ‬/ ‫ﻣﻔﻚ‬
signed rank test was used for comparing categorical
Farghaly et al. The Egyptian Journal of Neurology, Psychiatry and Neurosurgery (2021) 57:51 Page 4 of 8

Table 2 Comparison between MS patients versus healthy Test validity

controls on BICAMS The test time in HC ranged from 6 to 25 min with a me-
BICAMS subtests MS patients HC P value dian of 12 min (mean was 13.27 ± 4.22), and no statisti-
SDMT 39.2±13.3 50.9±10.8 <0.001* cally significant difference was found in time consumed
SDMT retest 42.7±15.1 57.1±11.2 <0.001* in test performance between control and MS patients in
which duration ranged from 7 to 50 min with median 14
Total CVLT-2 53.7±10.5 59.6± 8.5 <0.001*
min (mean was 14.95 ± 5.75).
Total CVLT-2 retest 61.6±10.1 66.24±8 <0.03*
All BICAMS subtests discriminated between MS pa-
Total BVMT-R 19.7± 9.2 25.4±8.7 <0.001* tients and HC (Table 2). MS patients scored significantly
Total BVMT-R 23.1± 10.3 31.8±4.9 <0.001* lower on the SDMT, CVLT total (TL), and BVRT-R
retest total (TL) tests compared to healthy controls with P
HC healthy control group, SDM Symbol Digit Modalities Test, CVLT-2 California values of <0.001, <0.001, and 0.001, respectively, which
Verbal Learning Test Second Edition, BVMT-R Brief Visuospatial Memory
Test Revised supports the validity of the Arabic BICAMS. BICAMS
*Statistically significant subtests were categorized as “impaired” and “not im-
paired”; with impairment defined as −1.5 SD below (cut-
off scores used were 34 in SDMT, 46 in CVLT TL, and
data, chi squared (χ2) test was performed. Exact test was 12 in BVRT-R TL). A significant number of MS patients
used instead when the expected frequency is less than 5. showed impairment in all BICAMS subtests in compari-
Correlations between quantitative variables were done son to controls; this was more pronounced in SDMT
using Spearman correlation coefficient. Correlation of where 31% of patients were affected (Table 3).
BICAMS test–retest scores was evaluated using Pearson Patients’ variables including age, education, disease
correlation coefficient r. P values less than 0.05 were duration, age of onset of disease, and disability measured
considered as statistically significant. by EDSS were tested in relation to performance of
BICAMS subtests (Table 4). Formal education level had
a significant influence on all BICAMS subtests; SDMT
Results (P=0.001), CVLT (P=0.014), and BVRT-R (P=0.02). Both
Patients with MS were matched with the HC group age of the patient and duration of illness affected pa-
with regard to age, sex, and years of education. There tients’ performance in SDMT and BVRT-R, but not in
were no significant differences between the MS and CVLT. On the other hand, the age of onset of disease
HC group on age (MS mean 30.8 years, SD 6.7, range had no significant impact on the performance of any test
19–52; HC mean 30.5 years, SD 7.9, range 19–52; P= in our sample. In addition, degree of disability correlated
0.41); gender (MS 70 females, 20 males; HC 60 fe- negatively with patients’ performance on the SDMT (P=
males, 25 males; P=0.22); or education (MS mean 0.001) and CVLT (P=0.007), but not BVRT-R (P=0.11).
14.5 years, SD 2.6, range 8–10; HC mean 14.3 years,
SD 3.3, range 11–24; P=0.21. Patients included were
76 (87.3%) diagnosed with relapsing remitting (RR) Test reliability
MS, 12 (13.3%) with secondary progressive (SP) MS, Test–retest reliability was assessed in all subjects who
and 2 (2.2%) with primary progressive (PP) MS. The were recruited for retest (Table 5). The test–retest
mean age of onset in patients was 25.24 (SD 7.1), reliability coefficients for each test were as follows:
while the mean disease duration was 6.2 (SD 5.8), SDMT: r = 0.85; CVLT-II: r = 0.65; and BVRT-R: r = 0.75
EDSS ranged from 1 to 6.5 with mean 2.8 (SD 1.8). (p < 0.0001).

Table 3 Comparison between frequency of impaired scores for MS patients and healthy controls on BICAMS subtests (using chi-
squared test)
BICAMS MS patients HC P
subtests (n=90) (n=85) value
Impaired Not impaired Impaired Not impaired
N (%) N (%) N (%) N (%)
SDMT 28 (31.1%) 62 (68.9%) 5 (5.8%) 81 (94.2%) <0.001*
Total CVLT-2 17 (19.5%) 70 (80.5%) 6 (7%) 80 (93%) 0.015*
Total BVMT-R 21 (23.9%) 67 (76.1%) 7 (8.1%) 79 (91.9%) 0.005*
HC healthy control group, SDMT Symbol Digit Modalities Test, CVLT-2 California Verbal Learning Test Second Edition, BVMT-R Brief Visuospatial Memory
Test Revised
*Statistically significant
Farghaly et al. The Egyptian Journal of Neurology, Psychiatry and Neurosurgery (2021) 57:51 Page 5 of 8

Table 4 Spearman’s correlations between clinical characteristics of the patients and BICAMS subtests
BICAMS test SDMT Total CVLT-2 learning trials Total BVMT-R learning trials
Correlation coefficient P value Correlation coefficient P value Correlation coefficient P value
Age −0.26 0.02* −0.17 0.31 −0.26 0.02*
Years of Education 0.36 0.001* 0.27 0.01* .0.25 0.02*
Age of onset of disease 0.002 0.99 0.006 0.96 −0.112 0.32
Duration of disease −0.41 <0.001* −0.18 0.11 −0.27 0.02*
EDSS −0.371 0.001* −0.31 0.007* −0.19 0.11
SDMT Symbol Digit Modalities Test, CVLT-2 California Verbal Learning Test Second Edition, BVMT-R Brief Visuospatial Memory Test Revised, EDSS Expanded
Disability Status Scale
*Statistically significant

Discussion different validation studies which ranged from 28 to 67%

BICAMS is a reliable and valid test that fills a gap in for SDMT; 20–73% CVLT total score and 10–58% for
neuropsychological assessment of patients with MS in BVRT total score [20, 24, 26, 28, 31]. In this study, 31%
Arabic speaking population, as proven by our results. It of patients showed impairment in SDMT, 20% CVLT
offers a rapid assessment tool, usually around 15 min, total score, and 21% for BVRT total score. A possible ex-
that is easily completed in an outpatient clinic by the planation is the younger age, shorter disease duration,
clinical staff. Translation and validation of the BICAMS and less disability in our patients. A recent study by
is established in several countries [19–35] which high- Hamdy and colleagues reported that the mean age of on-
lights its importance as a unified brief international as- set in Egypt is slightly lower than the reported estimates
sessment tool in patients with MS worldwide (Table 6). in the middle east and north Africa region (1); the mean
We found a significant difference between MS patients of age of patients included in this study is 30.8 (SD 6.7),
and HC group in all BICAMS Arabic version subsets (P which is younger than the mean of most previous valid-
value < 0.001). In this study, the level of education af- ation studies that ranged from 34 to 66.8 years (Table
fected the performance in all BICAMS Arabic version 6); also, the duration of illness was less than most other
subsets; also, the age of the patient, duration of illness, validation studies where mean duration of illness ranged
and level of disability (but not age of onset) contributed from 8 to 13.1 years while in our study mean disease
negatively to the performance on different tests. duration was 6.2 (SD 5.8); and mean EDSS in our study
All validation studies adopted the −1.5 SD of mean in was 2.8 (SD 1.8) while in other studies mean of EDSS
determining cut-off point apart from one study by ranged from 2.5 to 4.2 (Table 6).
Caneda and colleagues who used −1 SD for cut-off [23]. Variability in clinical characteristics of participants in
In our study, the cutoff scores according to 1.5 SD below different validation studies in addition to different lan-
the mean were 34 in SDMT, 46 in CVLT TL, and 12 in guages, ethnicity, nationality, and culture contributed to
BVMT-R TL; which is different from cut off points sug- the differences in results. Some of the differences be-
gested recently by Beier and colleagues for 1.5 SD below tween levels of impairment reported in different valid-
the mean which is 44 for SDMT; 39 for CVLT TL score ation studies can be explained by differences in the
and 17 for BVRT TL score [36]. Difference in cutoff validation sample, for example, our patient sample is
points used was subsequently associated with difference younger. However, despite the proven validity and reli-
in percent of patients impaired in tests observed in ability of BICAMS in all previous studies, individual

Table 5 Pearson’s correlation coefficients between the tests and the retests
Study subjects All subjects retested Patients Healthy controls
N=92 N=48 N=44
Test r P r P r P
SDMT 0.85 <0.001* 0.85 <0.001* 0.71 <0.001*
CVLT-II 0.65 <0.001* 0.61 <0.001* 0.63 <0.001*
BVMT-R 0.75 <0.001* 0.68 <0.001* 0.67 <0.001*
SDMT Symbol Digit Modalities Test, CVLT-2 California Verbal Learning Test Second Edition, BVMT-R Brief Visuospatial Memory Test Revised, EDSS Expanded
Disability Status Scale
*Statistically significant
Table 6 Previous studies validating BICAMS
Study country Czech Italy20,21 Brazil22 Brazil23* Lithuania24 Ireland25 Hungary26 Canada27 America28 Argentina29 Greece30# Belgium31 Turkey32 Portgal33 German34Ψ Japan35
Republic19
No. PwMS 369 192 58 34 50 67 65 57 41 50 44 97 173 105 172 156
HC 134 273 58 - 20 66 65 51 32 100 79 97 153 60 100 126
Age of PwMS (year) 34±10 41.4±10.8 41.2±12.2 43.4±10.8 38.8±10.2 43.9±12.1 41.9±8.9 45.4±9.9 46.7±8.6 43.4± 10.2 40.2±9.9 45.4±9.2 37.5 ± 10.7 38.3±11 43.3±11.6 41.4±9.3
Mean±SD
Years of education 14±3 12.3±3.5 12.7±5.2 15% ≤8 15.9±2.8 13.6±2.7 48% ≤12 15.44±2.7 15.2±2.2 14.9 ± 2.8 14.1±4.8 14.3±1.9 13.9 ± 7.3 13.6±3.7 - 14.1±1.9
Mean±SD 38% 8-11 52% ≥ 13
29% 11–
18
18% >18
Disease duration 8±7 12.7 ± 8.9 8.3±6.6 9.47±7.9 11.7±9.2 10.2± 8.4 11.1±7.6 10.1± 7.7 12.7±8.2 13.1±9.1 9.1±4.1 13± 7.2 9.2 ± 6.1 6.5 ±6 - 10.3±7.2
(year) Mean±SD/
Median
EDSS mean±SD 3±1.5 2.7±1.7 4.2±2 3.4±1.3 3.3±1.3 1.8±0.9 2.5±1.8 2.7± 1.9 - 3.3 ±2.6 3.5 3.5±2.5 2.4 ± 1.7 1.5 - 2.4±2.0
(RRMS)
5.7±1.4
(SPMS)
7 (PPMS)
SDMT HC Mean±SD 65± 9 56.3±11.3 47.5±13 56.3±10.3 57.7±11.5 55.9±10.9 66.8±12.4 59.1± 8.5 60.7±9.2 56.7± 10.9 61.4±13.1 61±10.2 53.5± 9.5 58.7 ±10 56.1±11.6 61.0±9.5
PwMS Mean±SD 50±13 46.4±12.8 35.9±16.1 48.5±14.9 42.7±13.9 46 ±12.9 55.6±15.5 49.7± 51.7±11.7 45.1±16.1 45.0±17.2 52.1±13.1 43.2 ± 51.8±11.2 47.4± 11.7 47.9±14
10.8 12.5 (BL)
% with 42 19 in all - 67 - - - 28.1 - - 43 - 41 14.3 19.2 -
impairment tests
CVLT HC Mean±SD 60±8 56.3± 9 58.4±8.3 65.7±5.9 52.8± 8.8 59± 8.3 57.7± 7.9 60.8±9 60.9± 10.5 60.5±10.7 61.3±9.7 53.9 ± 7.7 60.5±10 55.2± 10.3 55.7±
10.5
Farghaly et al. The Egyptian Journal of Neurology, Psychiatry and Neurosurgery

PwMS mean±SD 52±11 49.9±12.1 42.1 ± 48.2±8.6 55.9±10 45.3±10.2 55.4 ± 10.7 51.6± 53.6±10.9 50.9±12.4 55.5±12.3 60.1±12.9 45.7±11.3 55.1± 55.4±11.4 48.6±
12.4 10.1 11.9 (VLMT) 12.6
(BL)
% with 22 19 in all - 73 - 40 - 26.3 - - 20 - 38.2 9.5 8.1(on -
impairment tests VLMT)
BVRT HC mean±SD 29±4 27.9±6.1 23.8 ± 7.7 26.2±8.3 29.6±4.1 20.7± 6.6 26.7 ±5.6 29.8±3.6 25.7±6.3 23.4± 5.8 22.1±6.5 25.4±7.3 22.5±9.2 24.7 ± 5.5 27.4±6 28.3±5.4
(2021) 57:51

PwMS mean±SD 23±7 23.7±8 19.9 ± 8.6 23.5±6.7 23.1±7 17.9 ±7.1 22.54± 8.5 24.6±6.5 21.3±7 20.7±7.7 18.5±8.3 28.2±5.1 16.9 ± 8.5 21.7± 7.3 24.4±7.6 23.5±8.4
(BL)
% with 41 19 in all - 58 - 10 - 43.9 - - 22 33.5 11.4 26.5 -
impairment tests
*Used 1SD of the mean for cutoff and means of HCs were norms from previous studies
#Instead of the CVLT-II, the Greek Adaptation Greek Verbal Learning Test (GVLT) was used
Ψ
Instead of CVLT-II, the Rey Auditory Verbal Learning Test (RAVLT) German version: Verbaler Lern- und Merkfähigkeits-Test, (VLMT) was chosen as verbal short-term memory and learning test.
No. number, HC healthy controls, PwMS Patients with Multiple Sclerosis, EDSS Expanded Disability Status Scale, SDMT Symbol Digit Modality Test, CVLT California Verbal Learning Test, BVRT Brief Visuospatial Retention Test, BL baseline
RRMS relapsing remitting, MS SPMS secondary progressive, MS PPMS primary progressive MS
Page 6 of 8
Farghaly et al. The Egyptian Journal of Neurology, Psychiatry and Neurosurgery (2021) 57:51 Page 7 of 8

national validations of BICAMS according to language Received: 11 December 2020 Accepted: 29 March 2021
and culture are required [37].

References
Limitations
1. Hamdy SM, Abdel-Naseer M, Shalaby NM, Eelmazny AN, Nemr AA, Hassan A,
Many subjects dropped out in the retesting step which et al. Characteristics and predictors of progression in an Egyptian multiple
limited the test–retest comparisons. sclerosis cohort: a multicenter registry study. Neuropsychiatr Dis Treat. 2017;
13:1895–903. https://doi.org/10.2147/NDT.S140869.
2. El-Tallawy HN, Farghaly WMA, Badry R, Metwally NA, Shehata GA, Rageh TA,
Conclusion et al. Prevalence of multiple sclerosis in Al Quseir city, red sea governorate,
BICAMS Arabic version is a reliable and valid tool for Egypt. Neuropsychiatr Dis Treat. 2016;12:155–8. https://doi.org/10.2147/NDT.
S87348.
cognitive assessment of Arabic speaking MS patients in 3. Hashem S. MS in Egypt. Mult Scler Relat Disord. 2014;3(6):768–9. https://doi.
different clinical and research settings. org/10.1016/j.msard.2014.09.018.
4. Cutter GR, Baier ML, Rudick RA, Cookfair DL, Fischer JS, Petkau J, et al.
Abbreviations Development of a multiple sclerosis functional composite as a clinical trial
BICAMS: Brief International Cognitive Assessment for Multiple Sclerosis; outcome measure. Brain. 1999;122(Pt 5):871–82. https://doi.org/10.1093/bra
BRB: Brief Repeatable Battery; BVRT-R : Brief visuospatial retention test-revised; in/122.5.871.
BVRT TL: Brief visuospatial retention test total; CDE: Common Data Elements; 5. Prakash R, Snook E, Lewis J, Motl R, Kramer A. Cognitive impairments in
CVLT-II: California Verbal Learning Test 2nd edition; CVLT TL : California Verbal relapsing-remitting multiple sclerosis: a meta-analysis. Mult Scler J. 2008;
Learning Test Total; EDSS: Expanded Disability Status Scale; HC: Healthy 14(9):1250–61. https://doi.org/10.1177/1352458508095004.
control; MACFIMS: Minimal Assessment of Cognitive Function in MS; 6. Mollison D, Sellar R, Bastin M, Mollison D, Chandran S, Wardlaw J, et al. The
MS: Multiple sclerosis; MSFC: MS Functional Composite; NINDS: National clinico-radiological paradox of cognitive function and MRI burden of white
Institute of Neurological Disorders and Stroke; PP: Primary progressive; matter lesions in people with multiple sclerosis: a systematic review and
RR: Relapsing remitting; SDMT: Symbol Digit Modality Test; SP: Secondary meta-analysis. Aktas O, editor. PLoS One. 2017;12(5):e0177727.
progressive 7. Rao SM, Aubin-Faubert PS, Leo GJ. Information processing speed in patients
with multiple sclerosis. J Clin Exp Neuropsychol. 1989;11(4):471–7. https://
Acknowledgements doi.org/10.1080/01688638908400907.
None 8. Bever C, Grattan L, Panitch H, Johnson K. The brief repeatable battery of
neuropsychological tests for multiple sclerosis: a preliminary serial study.
Authors’ contributions Mult Scler J. 1995;1(3):165–9. https://doi.org/10.1177/135245859500100306.
MF: the idea, recruitment, the testing for patients and controls, data analysis, 9. Benedict RHB, Fischer JS, Beatty WW, Bobholz J, Chelune GJ, Langdon DW,
writing the manuscript. DL: the developer of the original test battery, et al. Minimal neuropsychological assessment of MS patients: a consensus
reviewed the manuscript. NS: recruitment, the testing for patients and approach. Clin Neuropsychol (Neuropsychology, Dev Cogn Sect D). 2002;
controls, writing the manuscript, submission. HS: distribution of roles, typing 16(3):381–97.
and distributing the test materials, recruitment, the testing for patients and 10. Erlanger DM, Kaushik T, Caruso LS, Benedict RHB, Foley FW, Wilken J, et al.
controls, study coordination. NA: recruitment, the testing for patients and Reliability of a cognitive endpoint for use in a multiple sclerosis
controls. AH: recruitment, the testing for patients and controls. MH: pharmaceutical trial. J Neurol Sci. 2014;340(1–2):123–9. https://doi.org/10.101
recruitment, the testing for patients and controls. AE: recruitment, the testing 6/j.jns.2014.03.009.
for patients and controls, SA: recruitment, the testing for patients and 11. NINDS. Summary of core/supplemental-highly recommended
controls, SS: data collection. AO: recruitment, the testing for patients and recommendations: multiple sclerosis CDEs multiple sclerosis version 1.1
controls. OY: recruitment, the testing for patients and controls. NK: idea, Start-up Resource-NINDS Multiple Sclerosis (MS) CDE Recommendations.
recruitment, the testing for patients and controls, writing manuscript. The 2018. Available from: https://www.commondataelements.ninds.nih.gov/Doc/
authors read and approved the final manuscript. MS/CDEStartupResource_MS.pdf
12. Langdon D, Amato M, Boringa J, Brochet B, Foley F, Fredrikson S, et al.
Recommendations for a Brief International Cognitive Assessment for
Funding
Multiple Sclerosis (BICAMS). Mult Scler J. 2012;18(6):891–8. https://doi.org/1
None
0.1177/1352458511431076.
13. Benedict RH, Amato MP, Boringa J, Brochet B, Foley F, Fredrikson S, et al.
Availability of data and materials Brief International Cognitive Assessment for MS (BICAMS): international
The datasets used and/or analyzed during the current study are available standards for validation. BMC Neurol. 2012;12(1):55 [cited 2017 Dec 5].
from the corresponding author on reasonable request. Besides, some data Available from: http://bmcneurol.biomedcentral.com/articles/10.1186/1471-
are available within the manuscript. 2377-12-55.
14. Smith A. Symbol Digit Modalities Test (SDMT). Manual (Revised). Los
Declarations Angeles: Western Psychological Services; 1982.
15. Delis D, Kramer J, Kaplan E, Ober K. California Verbal Learning Test – second
Ethics approval and consent to participate edition. Adult version. Manual. San Antonio: Psychological Corporation;
The study was approved by the local neurology ethical scientific committee, 2000.
Neurology Department, Cairo University, February 2017. 16. Benedict R. Brief Visuospatial Memory Test–Revised Professional manual.
All participants provided informed consent to all procedures. Odessa: Psychological Assessment Resources, Inc.; 1997.
17. Polman CH, Reingold SC, Banwell B, Clanet M, Cohen JA, Filippi M, et al.
Consent for publication Diagnostic criteria for multiple sclerosis: 2010 Revisions to the McDonald
Not applicable. criteria. Ann Neurol. 2011;69(2):292–302. https://doi.org/10.1002/ana.22366.
18. Sheridan LK, Fitzgerald HE, Adams KM, Nigg JT, Martel MM, Puttler LI, et al.
Competing interests Normative Symbol Digit Modalities Test performance in a community-based
The authors declare that they have no competing interests. sample. Arch Clin Neuropsychol. 2006;21(1):23–8. Available from: https://
www.sciencedirect.com/science/article/pii/S0887617705001174. https://doi.
Author details org/10.1016/j.acn.2005.07.003.
1
Neurology department, Kasr Al-Ainy School of Medicine, Al-Saraya St, 19. Dusankova JB, Kalincik T, Havrdova E, Benedict RHB. Cross cultural validation
Al-Manial district, Cairo, Egypt. 2Royal Holloway, University of London, of The Minimal Assessment of Cognitive Function in Multiple Sclerosis
Egham, Surrey TW20 0EX, UK. (MACFIMS) and The Brief International Cognitive Assessment for Multiple
 Farghaly et al. The Egyptian Journal of Neurology, Psychiatry and Neurosurgery (2021) 57:51 Page 8 of 8

Sclerosis (BICAMS). Clin Neuropsychol. 2012;26(7):1186–200. https://doi.org/1 Mult Scler J Exp Transl Clin. 2017;3(4):205521731774897 [cited 2018 Mar 25].
0.1080/13854046.2012.725101. Available from: http://journals.sagepub.com/doi/10.1177/2055217317748972.
20. Goretti B, Niccolai C, Hakiki B, Sturchio A, Falautano M, Minacapelli E, et al. 36. Beier M, Gromisch ES, Hughes AJ, Alschuler KN, Madathil R, Chiaravalloti N,
The brief international cognitive assessment for multiple sclerosis (BICAMS): et al. Proposed cut scores for tests of the Brief International Cognitive
normative values with gender, age and education corrections in the Italian Assessment of Multiple Sclerosis (BICAMS). J Neurol Sci. 2017;381:110–6.
population. BMC Neurol. 2014;14(1):171. https://doi.org/10.1186/s12883-014- https://doi.org/10.1016/j.jns.2017.08.019.
0171-6. 37. Smerbeck A, Benedict RHB, Eshaghi A, Vanotti S, Spedo C, Blahova
21. Niccolai C, Portaccio E, Goretti B, Hakiki B, Giannini M, Pastò L, et al. A Dusankova J, et al. Influence of nationality on the Brief International
comparison of the brief international cognitive assessment for multiple Cognitive Assessment for Multiple Sclerosis (BICAMS). Clin Neuropsychol.
sclerosis and the brief repeatable battery in multiple sclerosis patients. BMC 2018;32(1):54–62 Available from: http://www.ncbi.nlm.nih.gov/pubmed/2
Neurol. 2015;15(1):204. https://doi.org/10.1186/s12883-015-0460-8. 8721748.
22. Spedo CT, Frndak SE, Marques VD, Foss MP, Pereira DA, de F Carvalho L,
et al. Cross-cultural adaptation, reliability, and validity of the BICAMS in
Brazil. Clin Neuropsychol. 2015;29(6):836–46. https://doi.org/10.1080/1385404
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in
6.2015.1093173.
published maps and institutional affiliations.
23. Caneda MAG. de, Vecino MCA de. The correlation between EDSS and
cognitive impairment in MS patients. Assessment of a Brazilian population
using a BICAMS version. Arq Neuropsiquiatr. 2016;74(12):974–81. https://doi.
org/10.1590/0004-282x20160151.
24. Giedraitienė N, Kizlaitienė R, Kaubrys G. The BICAMS battery for assessment
of Lithuanian-speaking multiple sclerosis patients: relationship with age,
education, disease disability, and duration. Med Sci Monit. 2015;21:3853–9.
https://doi.org/10.12659/MSM.896571.
25. O’Connell K, Langdon D, Tubridy N, Hutchinson M, McGuigan C. A
preliminary validation of the brief international cognitive assessment for
multiple sclerosis (BICAMS) tool in an Irish population with multiple sclerosis
(MS). Mult Scler Relat Disord. 2015;4(6):521–5. https://doi.org/10.1016/j.msa
rd.2015.07.012.
26. Sandi D, Rudisch T, Füvesi J, Fricska-Nagy Z, Huszka H, Biernacki T, et al. 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(6):499–504. https://doi.org/10.1016/j.msard.2015.07.006.
27. Walker LAS, Osman L, Berard JA, Rees LM, Freedman MS, MacLean H, et al.
Brief International Cognitive Assessment for Multiple Sclerosis (BICAMS):
Canadian contribution to the international validation project. J Neurol Sci.
2016;362:147–52. https://doi.org/10.1016/j.jns.2016.01.040.
28. Goverover Y, Chiaravalloti N, DeLuca J. Brief International Cognitive
Assessment for Multiple Sclerosis (BICAMS) and performance of everyday
life tasks: actual reality. Mult Scler J. 2016;22(4):544–50. https://doi.org/10.11
77/1352458515593637.
29. Vanotti S, Smerbeck A, Benedict RHB, Caceres F. A new assessment tool for
patients with multiple sclerosis from Spanish-speaking countries: validation
of the Brief International Cognitive Assessment for MS (BICAMS) in
Argentina. Clin Neuropsychol. 2016;30(7):1023–31. https://doi.org/10.1080/13
854046.2016.1184317.
30. Polychroniadou E, Bakirtzis C, Langdon D, Lagoudaki R, Kesidou E, Theotokis
P, 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. https://doi.org/10.1016/j.msard.2016.06.011.
31. Costers L, Gielen J, Eelen PL, Van Schependom J, Laton J, Van Remoortel A,
et al. Does including the full CVLT-II and BVMT-R improve BICAMS?
Evidence from a Belgian (Dutch) validation study. Mult Scler Relat Disord.
2017;18:33–40. https://doi.org/10.1016/j.msard.2017.08.018.
32. Ozakbas S, Yigit P, Cinar BP, Limoncu H, Kahraman T, Kösehasanoğulları G.
The Turkish validation of the Brief International Cognitive Assessment for
Multiple Sclerosis (BICAMS) battery. BMC Neurol. 2017;17(1):208 [cited 2019
Feb 19]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/29207954
33. Sousa C, Rigueiro-Neves M, Miranda T, Alegria P, Vale J, Passos AM,
et al. Validation of the brief international cognitive assessment for
multiple sclerosis (BICAMS) in the Portuguese population with multiple
sclerosis. BMC Neurol. 2018;18(1):172 [cited 2019 Feb 19]. Available
from: https://bmcneurol.biomedcentral.com/articles/10.1186/s12883-018-
1175-4.
34. Filser M, Schreiber H, Pöttgen J, Ullrich S, Lang M, Penner IK. The Brief
International Cognitive Assessment in Multiple Sclerosis (BICAMS): results
from the German validation study. J Neurol. 2018;265(11):2587–93 [cited
2019 Feb 19]. Available from: http://link.springer.com/10.1007/s00415-018-
9034-1.
35. Niino M, Fukazawa T, Kira J, Okuno T, Mori M, Sanjo N, et al. Validation of
the Brief International Cognitive Assessment for Multiple Sclerosis in Japan.

View publication stats