arNIHSS - JNS 2015.pdf

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Foad Abd-Allah c, Mohammad A. FGamaleldin Osman b, Shady S. Geoa HealthPartners Clinics and Services Department of Neuroscb Ain Shams University Department of Neurology, Cairo, Egyc Cairo University, Kasralainy School of Medicine, Neurologyd Cedars-Sinai Department of Neurology, Los Angeles, CA, Un

ed in 1994 [4]. It hasials and practice [57].

Journal of the Neurological Sciences xxx (2015) xxxxxx

JNS-13921; No of Pages 5

Contents lists available at ScienceDirect

Journal of the Neur

j ourna l homepage: www.e1. Introduction trial [3]. The current version was rst publishsince become an integral part of stroke clinical trResults: In 6months, 137 patientswere recruited (mean age standard deviation 6212 years; 48women). Forinterrater agreement, weighted kappa value ranged from 0.36 to 0.66 and intraclass correlation coefcient (ICC)for the whole scale was excellent at 0.95 (95% condence interval [CI] 0.940.97). For intrarater agreement,weighted kappa ranged from 0.52 to 1.0 and the ICC was 0.94 (95% CI 0.870.98). The construct validity ofthe arNIHSS is demonstrated by its correlation with the DWI-ASPECT and the 3 months mRS score (Spearmancorrelation0.46 and 0.58 respectively; P b 0.001 for both).Conclusion: We developed and validated a culturally adapted Arabic version of the NIHSS. Further validation inother Arab countries is recommended.

2015 Elsevier B.V. All rights reserved.The original NIH Stroke Scale (NIHSS) wassity of Cincinnati [1,2] and subsequently mod

Funding source: None. Corresponding author at: HealthPartners Clinics a

St. Paul, MN 55130, United States.E-mail address: [email protected]

http://dx.doi.org/10.1016/j.jns.2015.07.0220022-510X/ 2015 Elsevier B.V. All rights reserved.

Please cite this article as: H.M. Hussein, et aNeurol Sci (2015), http://dx.doi.org/10.1016evaluated by correlating the arNIHSS on admission with the infarct volume on initial the diffusion weightedimaging (DWI) using the Alberta Stroke Program Early CT score (DWI-ASPECTS) and the functional outcomeat 3 months assessed by the modied Rankin Scale (mRS).Stroke severityArticle history:Received 5 March 2015Received in revised form 20 June 2015Accepted 10 July 2015Available online xxxx

Keywords:NIHSSCross-culturalTranslationArabicIschemic strokeNeurological examinationStroke scale

Introduction: The National Institutes of Health Stroke Scale (NIHSS), the most commonly used tool to quantifyneurological decit in acute stroke, was initially developed in English. We present our experience in developingand validating an Arabic version of the NIHSS (arNIHSS).Methods:

A) Scale development phase: 6 bilingual neurologists translated the scale to Arabic. Items 9 and 10 weremodied to suit the Arabic language and culture. A panel of 11 Arab neurologists reviewed the nal productand an Arabic language expert did nal editing.

B) Scale validation phase: 10 examiners (four neurology residents and six nurses), who had no experiencewith the NIHSS, were trained to use the arNIHSS. Patients with acute stroke were recruited at two academicinstitutions in Egypt. Each patient was examined on admission by 3 examiners using the arNIHSS and at24 hours by one of the three examiners. The agreement between the rst three examinations was used tocalculate the interrater agreement. The agreement between the admission and the 24-hour arNIHSS per-formed by the same examiner was used to calculate the intrarater agreement. Construct validity wasa b s t r a c ta r t i c l e i n f ol Moneim b, Tamer Emara b, Yousry A. Abd-elhamid b, Haitham H. Salem b,arrag c, M. Amir Tork b, Ali S. Shalash b, Khaled H. Ezz el dein b,rgy b, Peter G. Ghali b, Patrick D. Lyden d, Ramez R. Moustafa b

iences, St Paul, MN, United StatesptDepartment, Cairo, Egyptited StatesHaitham M. Hussein a,, Amr Abdeof Health Stroke Scale

Arabic cross cultural adaptation and validadeveloped at the Univer-ied for the NINDS rtPA

nd Services, 401 Phalen Blvd.,

om (H.M. Hussein).

l., Arabic cross cultural adapta/j.jns.2015.07.022on of the National Institutes

ological Sciences

l sev ie r .com/ locate / jnsUtilization of the NIHSS in non-English-speaking countries is chal-lenging. The difference in language may impair the examiner's abilityto understand the instructions. The objects used to test aphasia initem 9 may not be familiar in other cultures and the syllables used initem 10 maybe foreign or inadequate to test for dysarthria in languagesother than English. Several cross-cultural adaptations of the NIHSS haveaddressed these issues in their respective cultures [814].

tion and validation of the National Institutes of Health Stroke Scale, J

2 H.M. Hussein et al. / Journal of the Neurological Sciences xxx (2015) xxxxxxThe aim of this study was to develop an Arabic version of the NIHSS(arNIHSS). A culturally adapted Arabic version of the NIHSS is neededto serve more than 200 million Arabic native speakers; most of themdo not speak any other languages [15]. It will be particularly usefulin standardizing acute stroke care (initial assessment and monitoringof clinical progression) performed by neurologists as well as non-neurologists (other specialty physicians and non-physician providers).The non-neurologists group is important given the rarity of neurologistsin the Arab world, which has one neurologist per 100,000500,000population (much less than Europe and USAwhich have approximately4 per 100,000 population) [16].

2. Methods

The study was performed in 2 phases. Phase 1 was to develop thearNIHSS according to standard methods of cross-cultural adaptation[17,18], and phase 2 was to validate it in an Arabic speaking clinicalsetting.

2.1. Phase 1: arNIHSS scale development

Four bilingual neurologists translated the NIHSS to Arabic, creatingthe rst draft of the arNIHSS by consensus. A fth bilingual neurologistindependently back-translated the draft to English. Another investiga-tor compared theNIHSSwith the back translation andmade correctionsto the Arabic draft to reconcile discrepancies. The following changeswere made to items 9, aphasia, and 10, dysarthria (see online Supple-mentary material):

Cookie jar card: the word cookie on the jar was replaced by itsArabic equivalentObject naming card: the original cardwas replaced by the one devel-oped for the Spanish version of the NIHSS [10] because it has objectsthat are more familiar to natives of the Arabic world.Sentence reading card: except for minor modication in the order ofwords to fulll the proper Arabic grammar, the original sentenceswere translated word for word to maintain the meaning and theincremental complexity of the original version.Word reading card: we chose 6 words that would: a) test labial,lingual and glottal sounds, b) include the phonemes that are uniqueto the Arabic language, and c) be devoid of any cultural, social, orreligious insinuations.

To ensure that the scale was comprehensible and acceptable in thevarious Arab-speaking countries, the draft scale was sent to a panel ofeleven bilingual Arab neurologists from eight different Arab countries.Each neurologist independently reviewed and edited the draft. Thesechangeswere incorporated into one draft. Finally, an Arabic language ex-pert proofread the draft for spelling and grammar mistakes, producingthe nal version of the arNIHSS (online supplementarymaterial 1 and 2).

2.2. Phase 2: scale validation:

The goal of this phase was to assess a) the feasibility of trainingArabic speaking examiners to use the arNIHSS and b) the psychometriccharacteristics of the scale.

2.2.1. Training of examinersNeurology residents and nurses were approached to participate

in the study. Those who had previous experience with the NIHSS wereexcluded. Both study sites were allowed to design their own trainingprogram provided that they follow these guidelines: a) the trainingwould be provided by in Arabic by senior neurologists with exten-sive experience in NIHSS, and b) the training would consist of three

phases. Phase 1 involved explaining the purpose and use of the NIHSS,

Please cite this article as: H.M. Hussein, et al., Arabic cross cultural adaptaNeurol Sci (2015), http://dx.doi.org/10.1016/j.jns.2015.07.022examination techniques and scoring rules. Phase 2 focused on practic-ing the arNIHSS in groups and individually on actors with real timefeedback and discussion. Phase 3 allowed examiners to independentlypractice arNIHSS on actual stroke patients. Scores were reviewed andcorrected by the trainers. Examiners were admitted to the study whenat least 75% of their score was correct.

2.2.2. Study subjectsPatients 18 years or older who were admitted with ischemic stroke

to the stroke units of two academic institutions in Cairo, Egypt (AinShams University Hospital and Cairo University Hospital) were identi-ed. We excluded patients with hemorrhagic strokes, thrombolytictreatment, and onset N48 hours from presentation.

2.2.3. Study protocolEach patientwas examined on admission three separate times using

the arNIHSS by three different examiners. Each examinerwas blinded tothe scores given by the other examiners. A fourth examinationwas per-formed 24 hours later by one of those three examiners.

For patients with anterior circulation stroke, recruited at Ain ShamsUniversity Hospital, the diffusion weighted imaging (DWI) sequenceof the admission brain magnetic resonance imaging (MRI) was used tocalculate the infarct volume using themodication of the Alberta StrokeProgram Early CT score (DWI-ASPECTS) [19,20]. Modied Rankin Scale(mRS) was assessed through telephone interview at 3 months [21,22]by study investigators unaware of initial assessment. The proceduresfollowed in this study were in accordance of institutional guidelinesand the research authority at both academic institutions and hospitalsapproved the study. All patients (or their caregivers) consented to par-ticipate in the study.

2.2.4. Statistical analysisBaseline population characteristics were reported using frequency

for categorical variables, mean standard deviation (SD) for continu-ous variables, and median (interquartile range IQR) for nonparamet-ric variables. The initial three examinations were used to calculatethe interrater agreement. Weighted Kappa statistic was calculatedfor individual arNIHSS items, and was categorized as follows: poor ifb0.40, moderate if 0.40.75, and excellent if N0.75. If the kappa ofNIHSS item is included within the 95% CI of its corresponding item onthe arNIHSS, then the two kappaswere considered to be not statisticallydifferent. The two examinations done by the same examiner 24 hoursapart were used to calculate the intrarater agreement. The intraclasscorrelation coefcient (ICC) was also calculated but for the total scores.

To assess the construct validity of the arNIHSS, Spearman's correla-tion was calculated between arNIHSS (total and individual items) andDWI-ASPECTS, and between arNIHSS (total and individual items) andmRS. For the construct validity correlations, we calculated the averageof the initial three arNIHSS scores instead of choosing the scores givenby one examiner, since none of the initial scores represent the referenceor the gold standard.

All analytical procedureswere conducted using SPSS statistical pack-ages version 18 (SPSS Inc.) and SAS (PC SAS 9.2, SAS Institute Inc., Cary,North Carolina).

3. Results

3.1. Subjects' characteristics

A total of 137 patients were recruited into the study (mean age62 12 years; 48 women). Ain ShamsUniversity Hospital contributed117 patients and Cairo University Hospital contributed 20 patients(Table e-1). The median (IQR) arNIHSS score at admission and at24 hours was the same 5 (8). Median (IQR) DWI-ASPECTS (n = 68)was 7 (410). The median (IQR) mRS at 3 months (n = 117) was

2 (05).


agreement (Table 2). In comparison with the NIHSS, which had a

score was 0.94 (95% CI 0.870.98; Table 3) with no difference betweennurses 0.94 (95% CI 0.861.0) and physicians 0.91 (95% CI 0.810.99).

outcome at 3 months as measured by mRS (Spearman correlation 0.58;P b 0.001; Fig. 2).

Table 3Intrarater agreement of the arNIHSS.

Component Kappa(median)

Interquartilerange

Agreementbeyond chance

LOC (1a) 0.52 0.030.93 ModerateLOC questions (1b) 0.81 0.711.00 ExcellentLOC command (1c) 1.00 0.731.00 ExcellentGaze (2) 1.00 1.001.00 ExcellentVisual Fields (3) 0.63 0.420.95 ModerateFacial Weakness (4) 0.68 0.471.00 ModerateMotor left arm (5a) 0.79 0.620.85 ExcellentMotor right arm (5b) 0.65 0.450.95 ModerateMotor left leg (6a) 0.76 0.550.97 ExcellentMotor right leg (6b) 0.90 0.631.00 ExcellentAtaxia (7) 0.77 0.511.00 ExcellentSensory (8) 0.56 0.140.68 ModerateAphasia (9) 1.00 0.681.00 ExcellentDysarthria (10) 0.72 0.621.00 ModerateExtinction (11) 0.81 0.451.00 Excellent

ICC, Median Interquartile rangeTotal score 0.94 0.921.00 Excellent

arNIHSS: Arabic version of the NIH Stroke Scale; LOC: level of consciousness.

Table 1Distribution of responses for arNIHSS components by the initial three examinations.

Components Total responses(max = 411)

0 1 2 3 4

LOC (1a) 411 87.4 9.3 3.4 0 LOC questions (1b) 411 68.1 14.4 17.5 LOC Command (1c) 411 90.3 4.9 4.9 Gaze (2) 411 91.2 5.6 3.2 Visual Fields (3) 411 78.8 10.7 9.5 1 Facial Weakness (4) 411 34.1 45.3 18.2 1.5 Motor left arm (5a) 411 67.2 10.2 5.4 8.5 8.8Motor right arm (5b) 411 75.9 11.7 3.7 3.4 5.4Motor left leg (6a) 411 61.1 11 11.7 11 5.4Motor right leg (6b) 411 65.5 13.6 10.7 7.1 3.2Ataxia (7) 411 68.9 23.6 7.5 Sensory (8) 411 52.6 44 3.4 Aphasia (9) 408a 80.6 6.4 7.8 5.2 Dysarthria (10) 411 51.8 38.9 9.3 Extinction (11) 411 91.2 6.1 2.7

arNIHSS: Arabic version of the National Institutes of Health Stroke Scale; LOC: level ofconsciousness.

a Item was untestable in 3 patients.

3H.M. Hussein et al. / Journal of the Neurological Sciences xxx (2015) xxxxxxbroader distribution of agreement (2 excellent, 2 poor, and 11moderateagreement) the 95% CI of the kappa of all but three items of the arNIHSSoverlapped with the Kappa of the NIHSS: level of consciousnesscommands (item 1c) and visual eld (item 3) better interrater agree-ment in favor of NIHSS [23], and ataxia (item 7) in favor of arNIHSS.The ICC for the whole scale was excellent at 0.95 (95% CI 0.940.97),which is similar to the NIHSS ICC of 0.94 (95% CI 0.841.00) [23].Six nurses and four neurology residents were recruited to the study(Table e-2). There were 411 responses recorded for each of the scaleitems on admission (137 patients 3 examiners) except for item9 (aphasia) for which only 408 responses were recorded because ofintubation of one patient. Responses distributed throughout all possiblelevels for all items except level 3 for item 1a (see Table 1). At 24 hours,110 responses were available for each item.

3.2. Interrater agreement

The three independent examinations performed on the rst dayof admission, had kappa value for interrater agreement ranging from0.36 to 0.66. One itemwas categorized as poor agreement (facial weak-ness), and the rest of the fourteen items were categorized as moderateTable 2Interrater agreement of the arNIHSS compared with NIHSS.

Kappa (95%CI)

Components arNIHSS (95% CI) Agreement ca

LOC (1a) 0.61 (0.53, 0.69) ModerateLOC questions (1b) 0.64 (0.56, 0.72) ModerateLOC Command (1c) 0.58 (0.50, 0.66) ModerateGaze (2) 0.42 (0.34, 0.49) ModerateVisual Fields (3) 0.44 (0.36, 0.52) ModerateFacial Weakness (4) 0.36 (0.28, 0.44) PoorMotor left arm (5a) 0.57 (0.51, 0.63) ModerateMotor right arm (5b) 0.66 (0.60, 0.72) ModerateMotor left leg (6a) 0.61 (0.55, 0.67) ModerateMotor right leg (6b) 0.56 (0.50, 0.62) ModerateAtaxia (7) 0.41 (0.33, 0.49) ModerateSensory (8) 0.51 (0.43, 0.59) ModerateAphasia (9) 0.64 (0.58, 0.70) ModerateDysarthria (10) 0.53 (0.45, 0.61) ModerateExtinction (11) 0.55 (0.47, 0.63) Moderate

ICC (95%)Total scores 0.95 (0.94, 0.97) Excellent

arNIHSS: Arabic version of the NIH Stroke Scale; CI: condence interval; LOC: level of consciou

Please cite this article as: H.M. Hussein, et al., Arabic cross cultural adaptaNeurol Sci (2015), http://dx.doi.org/10.1016/j.jns.2015.07.022We performed a comparison of individual items and total score by spe-cialty (physician versus nurses) and even compared individual exam-iners; however, we did not nd statistically signicant differences.

3.4. Construct validity

The construct validity of the arNIHSS is demonstrated by thecorrelation between the average of the three initial arNIHSS assess-ments with the infarct volume on MRI using the DWI-ASPECTS (Spear-man correlation 0.46; P b 0.001; Fig. 1) and with the functional3.3. Intrarater agreement

One hundred and ten patients were examined a second time by thesame examiner, 24 hours after the initial examination. Kappa forintrarater agreement ranged from0.52 to 1.0. The agreementwas excel-lent for nine items and moderate for six items. The ICC of the overalltegory NIHSS (95% CI) [23] Agreement category

0.46 (0.39, 0.53) Moderate0.77 (0.64, 0.90) Excellent0.92 (0.75, 1.0) Excellent0.70 (0.39, 1.0) Moderate0.72 (0.57, 0.87) Moderate0.38 (0.27, 0.49) Poor0.65 (0.51, 0.79) Moderate0.72 (0.54, 0.79) Moderate0.64 (0.53, 0.72) Moderate0.64 (0.53, 0.72) Moderate0.21 (0.12, 0.30) Poor0.73 (0.53, 0.93) Moderate0.64 (0.53, 0.75) Moderate0.56 (0.39, 0.73) Moderate0.57 (0.40, 0.74) Moderate

0.94 (0.84, 1.00) Excellent

sness.


Fig. 1. arNIHSS according to DWI-ASPECTS. The construct validity of the arNIHSS is dem-onstrated by the incremental increase in the median of the average of the three baselineassessments, indicating more severe neurologic decit, as the DWI-ASPECTS scoredecreases, indicating larger infarct volume. arNIHSS: Arabic version of the NationalInstitutes of Health Stroke Scale; DWI: diffusion weighted imaging; ASPECTS: AlbertaStroke Program Early CT score.

4 H.M. Hussein et al. / Journal of the Neurological Sciences xxx (2015) xxxxxx4. Discussion

Our study design is similar to the Thai version of the NIHSS [11]in which the examiners were practicing nurses and physicians (notneurologists with long clinical experience as in the Spanish version[10]) and the patients were actual patients of those examiners (versusvideotaped cases as in the NIHSS [23] and the Italian version [13]).This design makes our study more representative of real life trainingand patient care encounters rather than ideal educational conditions.

The difference in methods probably accounts for some of the differ-ences in results when our study is compared to previous studies. Whilethe NIHSS items analysis used unweighted kappa, we did use weightedkappa since it is the more suitable to compare ordinal variables. All theitems in which interrater agreement was categorized as moderate bythe NIHSS were similarly categorized as moderate by the arNIHSS. Thedifference between the two scales is in three items that were catego-rized as moderate by the arNIHSS, while categorized as excellent(items 1b and 1c) or poor (item 7) by the NIHSS. The random patientselection and the variablemixes of examiners (every patient was exam-ined by any 3 out of the 10 examiners, but not all examiners examinedeach patient) may have brought the agreement to a realistic middlerather than extreme values. Another contributing factor is the acuityof the cases, as the patients had suffered an acute stroke 48 hoursprior to study participation. In this acute stage, patients' neurologicalstate, particularly the level of consciousness, may uctuate for a varietyof medical reasons. This is in contrast to the NIHSS in which 26 patientswere selected from stroke clinics andwere sent to a professional TV stu-dio to optimize videotaping quality and then the interrater agreement isFig. 2. arNIHSS according tomRS. The construct validity of the arNIHSS is demonstrated bythe incremental increase in the median of the average of the three baseline assessments,indicatingmore severe neurologic decit, as the 3-monthsmRS score increases, indicatingmore severe disability. arNIHSS: Arabic version of the National Institutes of Health StrokeScale; mRS: modied Rankin Scale.

Please cite this article as: H.M. Hussein, et al., Arabic cross cultural adaptaNeurol Sci (2015), http://dx.doi.org/10.1016/j.jns.2015.07.022derived from all examiners who reviewed the same video clip of theitem examined [23]. In developing the Spanish version NIHSS, onlytwo examiners examined the patients and the statistical analysis wasbased on the score values obtained by them.

Comparing the current study to other NIHSS-validation studies,this study used dual indicators for construct validity while other studiesused only functional outcome scales. The construct validity of thearNIHSS has a signicant correlation for both DWI-ASPECTS and func-tional outcome at 3 months as measured by mRS. Its correlation withboth radiological and clinical marker indicates that arNIHSS versionfunctioned as it was hypothesized.

The NIHSS itself has well recognized limitations, which led to thedevelopment of the modied NIHSS (mNHISS) trying to eliminate theitems with low reliability: level of consciousness, facial palsy, limbataxia, and dysarthria [24]. The arNIHSS shares the same limitationsfor facial palsy and limb ataxia, and dysarthria, performs better thanNIHSS in level of consciousness, and worse in visual eld and gazeitems. An exploration into a modied arNIHSS is warranted to assesswhether it will increase the reliability. The intrarater reliability in thisstudy was undertaken by comparing individual rater's arNIHSS exami-nation of the same patient on admission and at 24 hours. The assump-tion was that the change in neurological state would not cause asignicant change in the arNIHSS score over this time period for thevastmajority of patients. Tominimize the chance of a signicant changein the arNIHSS, we excluded patients whowere treated with thrombol-ysis and we limited the time period between the rst and the secondexamination to 24 hours. This method was used in the validation ofthe Spanish version of the NIHSS [10].

In the Arab world, NIHSS has always been taught in English and leftto the individual to create his/her own Arabic version for their practice.We are aware of several attempts by individuals and institutions tocreate an Arabic version of the NIHSS, yet these versions were not vali-dated and remained local. The arNIHSS is an opportunity to standardizethe utilization of the NIHSS among Arabic-speaking populations. Theinclusion of a panel of neurologists from all over the Arab world in thedevelopment of the scale aimed at this pan-Arab goal. However, thevalidation phase was implemented only in Egypt on Egyptian patients.Future validation in other Arabic-speaking countries is needed to ensurethat the current arNIHSS version is universally pertinent. Anotherpotential limitation is the lack of a unied training program, whichcan potentially improve the interrater agreement. Creating a certica-tion process will ensure the standardization of instructions and therigor of training. Further work should be directed at new training strat-egies using in-print and online materials to increase the utilization ofarNIHSS.

5. Conclusion

A culturally adaptedArabic version of theNIHSS has beendeveloped.The proposed version has been found to be valid and reliable using acohort in Egypt. Validation in other Arab countries is recommended.

Acknowledgment

Panel of bilingual Arab Neurologists by country of origin:Tunisia: Senda Ajroud-Driss MD (Chicago, IL), Nizar Souayah MD

(Newark, NJ)Sudan: Khalafallah Bushara, MD (Minneapolis, MN)Lebanon: Mustapha Ezzeddine MD (Minneapolis, MN), Gamil Fteeh

MD (Houston, TX)Syria: Yousef Hennawi MD (Houston, TX), Amrou Serajj MD

(Houston, TX)Palestine: Akram Shehadeh MD (Milwaukee, WI)Saudi Arabia: Amer Zahrallayalli MD (Houston, TX)Jordan: Osama Zaidat MD (Milwaukee, WI)

Iraq: Saef Ahmed MD (Boston, MA)


Professional ArabicEnglish TranslatorMr Suhaib Alrawi (Houston, TX)

Appendix A. Supplementary data

Supplementary data to this article can be found online at http://dx.doi.org/10.1016/j.jns.2015.07.022.

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5H.M. Hussein et al. / Journal of the Neurological Sciences xxx (2015) xxxxxxPlease cite this article as: H.M. Hussein, et al., Arabic cross cultural adaptaNeurol Sci (2015), http://dx.doi.org/10.1016/j.jns.2015.07.022tion and validation of the National Institutes of Health Stroke Scale, J

Arabic cross cultural adaptation and validation of the National Institutes of Health Stroke Scale1. Introduction2. Methods2.1. Phase 1: arNIHSS scale development2.2. Phase 2: scale validation:2.2.1. Training of examiners2.2.2. Study subjects2.2.3. Study protocol2.2.4. Statistical analysis

3. Results3.1. Subjects' characteristics3.2. Interrater agreement3.3. Intrarater agreement3.4. Construct validity

4. Discussion5. ConclusionAcknowledgmentAppendix A. Supplementary dataReferences

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arNIHSS - JNS 2015.pdf