Diagnostic Accuracy of Mini-Mental Status Examination and Revised Hasegawa Dementia Scale for Alzheimer s Disease
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1 Originl Reserch Article Dement Geritr Cogn Disord 2005;19: DOI: / Accepted: Novemer 1, 2004 Pulished online: Mrch 22, 2005 Dignostic Accurcy of Mini-Mentl Sttus Exmintion nd Revised Hsegw Dementi Scle for Alzheimer s Disese K.W. Kim, c D.Y. Lee, c J.H. Jhoo e J.C. Youn f Y.J. Suh d, g Y.H. Jun E.H. Seo d, c, d J.I. Woo Deprtment of Neuropsychitry, Seoul Ntionl University Bundng Hospitl, Seongnm-si, Gyeonggi-do ; Deprtment of Neuropsychitry, Seoul Ntionl University Hospitl; c Seoul Ntionl University College of Medicine, nd d Clinicl Reserch Institute of Seoul Ntionl University Hospitl, Seoul; e Deprtment of Neuropsychitry, Pundng Jeseng Hospitl, Dejin Medicl Center, Seongnm-si, nd f Deprtment of Neuropsychitry, Kyunggi Provincil Hospitl for the Elderly, Yongin-si, Gyeonggi-do ; g BK21 Reserch Division for Humn Life Science, Seoul Ntionl University, Seoul, Kore Key Words Revised Hsegw Dementi Scle Mini-Mentl Sttus Exmintion Dignostic ccurcy Alzheimer s disese Eduction Severity Astrct To compre the dignostic ccurcies of the Revised Hsegw Dementi Scle (HDS-R) nd Mini-Mentl Sttus Exmintion (MMSE) for Alzheimer s diseses (AD), we dministered them simultneously to 82 AD ptients nd 82 ge- nd sex-mtched nondemented control sujects. The re under the receiver opertor curve (AUC) for AD of the HDS-R (AUC HDS-R ) nd MMSE (AUC MMSE ) were igger thn 0.90 indicting tht oth tests re useful for detecting AD. However, AUC HDS-R (0.952) ws significntly lrger thn tht of the AUC MMSE (0.902) regrdless of the eductionl level of the sujects, indicting tht the HDS-R is more ccurte thn MMSE in dignosing AD. Moreover, the superiority of the HDS-R (AUC HDS-R = 0.894) to the MMSE (AUC MMSE = 0.704) remined significnt in mild AD ptients lone, who re the focus of screening. In conclusion, the HDS-R is etter thn the MMSE s screening instrument for AD. Introduction As the prevlence of Alzheimer s disese (AD) increses nd the interventions for it ecome ville, there is n incresing need for ccurte screening tests which cn prompt the erly detection of AD. Currently, vrious ptient-sed tests including the Alzheimer s Disese Rting Scle (ADAS) [1], Mttis Dementi Rting Scle (MDRS) [2], Mini-Mentl Sttus Exmintion (MMSE) [3], nd Revised Hsegw Dementi Scle (HDS-R) [4] re in use for screening AD ptients. Idelly, the tests for screening AD should e sensitive nd specific enough to identify cognitively impired individuls who need further comprehensive evlution nd mngement. At the sme time, they could e quickly nd esily dministered not only y physicins ut lso y nurses or other trined helth personnel. In this sense, the ADAS nd MDRS, lthough they hve high sensitivity for AD [1, 5], re too long to e quickly dministered s screening instruments. It tkes out min to dminister the ADAS or MDRS to suject [6]. Moreover they require too much clinicl judgment to e esily dministered y riefly trined nonphysicin personnel. Thus, the rief screening tests such s Copyright 2005 S. Krger AG, Bsel Fx E-Mil krger@krger.ch S. Krger AG, Bsel /05/ $22.00/0 Accessile online t: Jong-Inn Woo, MD, PhD, Deprtment of Neuropsychitry Seoul Ntionl University, College of Medicine nd Seoul Ntionl University Hospitl 28 Yongon-dong, Chongno-gu, Seoul (Kore) Tel , Fx E-Mil jiwoomd@plz.snu.c.kr
2 the MMSE nd HDS-R, which tke less thn 15 min for dministrtion, re more widely used in primry cre settings nd epidemiologicl studies thn the ADAS or MDRS. The MMSE hs een used most widely for screening cognitive impirment including dementi. However, since it ws originlly developed to evlute elderly psychitric ptients rther thn dementi ptients, it is criticized for its level of sensitivity nd specificity for dementi [7, 8]. In ddition, its insensitivity to frontl dysfunction limits further the usefulness s screening test for dementi. The HDS-R, however, lthough it hs een used exclusively in Est Asin countries till now, hs some dvntges s screening test for AD compred to MMSE. Although it consists of nine simple questions, it cn evlute the frontl function s well s orienttion, memory, nd ttention. Furthermore, it could e dministered to the disled elderly who hve motor impirment since it does not contin ny performnce test such s visuosptil ility nd prxis. In the present study, we compred the dignostic ccurcies of the MMSE nd HDS-R for AD y dministering them simultneously to the sme popultion so tht clinicins my choose the etter screening test for AD. Methods Sujects All the sujects were enrolled from the Dementi Specil Clinics in Seoul Ntionl University Hospitl, Seoul Ntionl University Bundng Hospitl, nd Kyunggi Provincil Hospitl for the Elderly nd two community-sed cohorts (Kwnkgu, Junggu) in Seoul, Kore. They were 50 yers old or older, speking Koren, nd hd dequte vision nd hering, lthough mny wore glsses nd some required hering id. Illiterte persons were excluded ecuse they were unle to red the word lists in the tests. The sujects who hd serious medicl, psychitric, or neurologicl disorders tht could ffect mentl function were lso excluded. However, the sujects with minor physicl normlity (e.g. dietes with no serious compliction, essentil hypertension, mild hering loss, etc.) were not excluded. Conforming to the protocol of the Koren version of the CERAD clinicl ssessment ttery (CERAD-K) [9], ech suject ws exmined y neuropsychitrist with dvnced trining in dementi reserch. The sujects with prole or possile AD were enrolled in the ptient group. The dignosis of dementi ws mde ccording to the criteri from the 4th edition of the Dignostic nd Sttisticl Mnul of Mentl Disorders [10], nd the dignosis of AD ws mde ccording to the criteri proposed y the Ntionl Institute of Neurologicl nd Communictive Disorders nd Stroke/ Alzheimer s Disese nd Relted Disorders Assocition [11]. The sujects who were dignosed s cognitively norml y the CERAD-K clinicl ssessment were enrolled in the nondemented control group. All the control sujects were functioning independently in the community nd did not hve cognitive impirment tht ltered their dily ctivities. The Blessed Dementi Scle [9] scores of ll of them were 0. The ge ( 8 1 yer) nd sex of the control sujects were mtched to those of the AD ptients. Neuropsychologicl Assessment Eight trined nurses dministered the Koren versions of MMSE [9] nd HDS-R [12] simultneously to ech suject. They were linded to the dignosis. To stndrdize the dministrtion nd to ensure uniformity of dt gthered, we mde n instruction mnul nd trined the nurses to conform to it. In the Koren version of the MMSE, the items for reding nd writing in the originl version were replced y two items focusing on judgment since there re significnt numer of illiterte people in Kore. The glol severity of dementi ws determined ccording to the Clinicl Dementi Rting (CDR). Sttisticl Anlysis The eductionl levels of the AD ptients nd control sujects were compred y Student t test or Mnn-Whitney U test when pproprite. The men scores of the MMSE nd HDS-R of the AD ptients nd control sujects were compred y ANOVA, computing the level of eduction s covrite. The correltions mong the MMSE nd HDS-R scores were exmined y two-tiled Person correltion test, nd the correltions of the HDS-R nd MMSE scores with the CDR were exmined y the Spermn rnk-order correltion test. The optiml cut-off scores stisfying oth sensitivity nd specificity for AD were determined y the ROC nlyses. To mesure the dignostic ccurcy of ech test for AD, the re under the ROC curves (AUCs), the stndrd errors (SEs), nd the 95% confidence intervl (95% CI) were clculted. The AUC is rnged etween 0.5 nd 1; the nerer to 0.5 the less ccurcy it hs ut the nerer to 1 the more ccurcy it hs. To exmine the difference in the dignostic ccurcy of the MMSE nd HDS-R for AD, we compred the AUC y clculting criticl rtio z proposed y Hnley nd McNeil [13] in The z ws defined s: z A _ 1 A2 SE SE _ 2rSE SE where A 1 nd SE 1 refer to the oserved AUC nd estimted SE of the AUC ssocited with test 1, A 2 nd SE 2 refer to the oserved AUC nd estimted SE of the AUC ssocited with test 2, nd r refers to the estimted correltion coefficient etween A 1 nd A 2. Note tht the z follows the stndrd norml distriution. All the sttisticl nlyses were done using SPSS 10.0 nd SAS 8.1. Dignostic Accurcy for AD of MMSE nd HDS-R Dement Geritr Cogn Disord 2005;19:
3 Tle 1. Chrcteristics of Alzheimer s disese ptients nd norml control sujects Control sujects AD ptients ll low eduction high eduction ll low eduction high eduction Numer Age, yers (57 87) (58 87) (57 80) (56 88) (57 88) (56 83) Eduction, yers (0 19) (0 6) (8 19) (0 18) (0 6) (9 18) Gender, % femle Men 8 stndrd devition (minimum mximum). The sujects educted 6 yers or less were clssified s low-eduction group, nd those educted 7 yers or more were clssified s high-eduction group. Tle 2. The men scores of the Mini- Mentl Sttus Exmintion (MMSE) nd Revised Hsegw Dementi Scle (HDS-R) strtified y the dignosis nd Clinicl Dementi Rting (CDR) Dignosis Numer MMSE HDS-R Control sujects (CDR = 0) (17 29) (12 28) AD ptients All (2 28) (0 26) Mild (CDR = 0.5 or 1.0) (9 28) (5 26) Moderte (CDR = 2.0) (6 14) (2 17) Severe (CDR = 3.0) (2 9) (0 8) Men 8 stndrd devition (minimum mximum). The MMSE nd HDS-R scores of control sujects were significntly different from those of AD ptients; F(1,162) = , p < for the MMSE nd F(1,162) = , p < for the HDS-R y eduction-djusted ANOVA. The men scores of the MMSE nd HDS-R were significntly different ccording to the CDR; F(2,79) = 27.37, p < for the MMSE nd F(2,79) = 25.33, p < for the HDS-R y the eduction-djusted ANOVA. Results In this study, 82 AD ptients nd 82 ge- nd sexmtched nondemented control sujects were exmined. As presented in tle 1, there ws no significnt difference in the eductionl level distriution etween the AD ptients nd control sujects (p y Student t test), which ws the cse either in the low-eduction group (educted 6 yers or less) or in the high-eduction group (educted 7 yers or more). Tle 2 summrized the men scores of the MMSE nd HDS-R from the AD ptients nd control sujects. The AD ptients performed significntly worse thn the control sujects in the two tests (p! y the level of eduction-djusted ANOVA). The performnce of ech test ws lso significntly influenced y the severity of AD. The severer the AD, the lower ws the score of ech test (p! y the level of eduction-djusted ANOVA). The Spermn s correltion coefficients of the MMSE nd HDS-R with severe AD (n = 82) were nd 0.701, respectively. The scores of the MMSE nd HDS-R were lso highly correlted with ech other; Person correltion coefficient ws etween the MMSE nd HDS-R (d.f. = 162, p! ). Those correltions remined significnt when the AD ptients nd control sujects were nlyzed seprtely. The Person correltion coefficient etween the MMSE nd HDS-R ws (d.f. = 80, p! ) in the AD ptients, nd etween the MMSE nd HDS-R (d.f. = 80, p! ) in the norml controls. The correltion coefficient in the AD group is significntly higher thn tht in the norml controls (z = 3.29, p = y the test of compring correltions using the Fisher s z-trnsformtion). The results of ROC nlyses for AD re summrized in tle 3. The optiml cut-off scores of the MMSE nd HDS-R were determined s 20/21 nd 17/18, respectively. The 95% CI do not incorporte 0.5 in oth tests, show- 326 Dement Geritr Cogn Disord 2005;19: Kim/Lee/Jhoo/Youn/Suh/Jun/Seo/Woo
4 Tle 3. Receiver opertor curve (ROC) nlyses of the Mini-Mentl Sttus Exmintion (MMSE) nd Revised Hsegw Dementi Scle (HDS-R) for Alzheimer s disese Cut-off Sensitivity Specificity AUC AUC SE 95% CI MMSE / / / HDS-R / / / AUC = Are under the ROC; SE = stndrd error; 95% CI = 95% confidence intervl. Optiml cut-off scores for Alzheimer s disese y ROC nlyses. Tle 4. Receiver opertor curve (ROC) nlyses of the Mini-Mentl Sttus Exmintion (MMSE) nd Revised Hsegw Dementi Scle (HDS-R) for mild Alzheimer s disese Cut-off Sensitivity Specificity AUC AUC SE 95% CI MMSE / / / HDS-R / / / AUC = Are under the ROC; SE = stndrd error; 95% CI = 95% confidence intervl. Optiml cut-off scores for mild Alzheimer s disese y ROC nlyses. ing tht they predict AD etter thn chnce. The sensitivity nd specificity for AD of the MMSE were nd 0.878, respectively, t its optiml cut-off, which were comprle to those previously reported [14]. The sensitivity nd specificity for AD of the HDS-R t its optiml cut-off were higher thn those of the MMSE; the sensitivity ws nd specificity ws In the logistic regression nlyses djusting the level of eduction, 84.8 nd 91.5% of dignoses were correctly predicted y the MMSE nd HDS-R, respectively, t their optiml cutoffs. As shown in tle 3, the AUCs of the MMSE (AUC MMSE ) nd HDS-R (AUC HDS-R ) were igger thn 0.90 indicting tht oth tests re useful for detecting AD. However, the AUC HDS-R ws igger AUC MMSE, nd the difference ws sttisticlly significnt (z = 2.19, p = 0.014), indicting tht the HDS-R is more ccurte thn MMSE in dignosing AD. Then we performed the ROC nlyses gin for mild AD ptients only, since ll the flse negtive ptients were mild (CDR = 0.5 or 1) in the present study nd moderte to severe AD ptients re not the focus of screening. The optiml cut-off scores of the MMSE nd HDS-R for mild AD were 20/21 nd 18/19, respectively ( tle 4 ). At their optiml cut-off points, 75.2 nd 83.8% of dignoses were correctly predicted y the MMSE nd HDS-R, respectively (y the level of eduction-djusted logistic regression nlysis). As expected, the dignostic ccurcies of the MMSE nd HDS-R were rought down to nd 0.894, respectively. However, the HDS-R still showed Dignostic Accurcy for AD of MMSE nd HDS-R Dement Geritr Cogn Disord 2005;19:
5 Tle 5. Receiver opertor curve (ROC) nlyses of the Mini-Mentl Sttus Exmintion (MMSE) nd Revised Hsegw Dementi Scle (HDS-R) for Alzheimer s disese strtified y the level of eduction Cut-off Sensitivity Specificity AUC AUC SE 95% CI Low-eduction group MMSE / / / HDS-R / / / High-eduction group MMSE /22* / / HDS-R /18** / / AUC = Are under the ROC; SE = stndrd error; 95% CI = 95% confidence intervl. Optiml cut-off scores for mild Alzheimer s disese y ROC nlyses. The sujects educted 6 yers or less were clssified s low-eduction group, nd those educted 7 yers or more were clssified s high-eduction group. * There ws no suject who scored 21 in MMSE. ** There ws no suject who scored 17 in HDS-R. higher sensitivity nd specificity thn MMSE in detecting mild AD. The AUC HDS-R ws lrger thn AUC MMSE indicting tht the HDS-R my e etter thn the MMSE in detecting mild AD. The difference etween the AUC HDS-R nd the AUC MMSE ws sttisticlly significnt (z = 3.85, p! ). We nlyzed the dignostic ccurcies of the MMSE nd HDS-R in the low- nd high-eduction group seprtely, since the performnce of ech test ws significntly correlted with the level of eduction (r = 0.412, d.f. = 162, p! for the MMSE; r = 0.259, d.f. = 162, p = for the HDS-R y Person correltion tests). In the low-eduction group, the optiml cut-off scores of the MMSE nd HDS-R for AD were determined s 16/17 nd 15/16, respectively, t which 93.9 nd 92.2% of the dignoses were correctly predicted, respectively. In the high-eduction group, the optiml cut-off scores of the MMSE nd HDS-R for AD were determined s 22/23 nd 18/19, respectively, t which 75.5 nd 89.8% of the dignoses were correctly predicted, respectively. As shown in tle 5, the AUC HDS-R ws significntly lrger thn AUC MMSE in the low-eduction group (z = 2.23, p = 0.013) s well s in the high-eduction group (z = 2.94, p = 0.002) indicting tht the HDS-R my e etter in detecting AD thn the MMSE regrdless of the eductionl level of sujects. Discussion This study ws undertken to compre the ccurcies of the MMSE nd HDS-R in dignosing AD. While previous pulictions supported the vlidity nd reliility of the two tests for AD [4, 9], their dignostic ccurcies for AD hve not een compred with ech other. In the present study, we compred the dignostic ccurcy not only y the sensitivity nd specificity ut lso y AUC. Although the ssessment of dignostic ccurcy using sensitivity nd specificity re commonly used, it is dequte only when the decision criterion such s cut-off 328 Dement Geritr Cogn Disord 2005;19: Kim/Lee/Jhoo/Youn/Suh/Jun/Seo/Woo
6 score is greed upon nd invrint. Moreover the decision criterion is susceptile to the differences in the chrcteristics of study smple. For exmple, the sensitivity nd specificity of the MMSE were vrying from 71 to 92% nd from 51 to 96% respectively [15]. The optiml cut-off score of the HDS-R for dementi ws 20/21 in Jpnese popultion with sensitivity of 0.90 nd specificity of 0.82 [4], while 15/16 in Koren popultion with sensitivity of 0.95 nd specificity of 0.91 [12]. In contrst, the AUC is independent of the decision criterion nd less contminted y the extrneous fctors tht ffect the response, lthough it is neither perfectly relile nor perfectly vlid, since it is not free from the influences of the version or dministrtion procedure of n instrument. This is why the AUC cn provide etter mesure of predictive ccurcy thn the sensitivity nd specificity. Our results indicted tht the HDS-R did etter thn MMSE, hving the lrger AUC s well s the higher sensitivity nd specificity for AD regrdless of severity nd eductionl level of the sujects. Thus the superiority of the HDS-R to MMSE my e minly ttriuted to the difference in the cognitive mesures included in ech test. The HDS-R hs cognitive mesures tht re not enough or not included t ll in the MMSE. The HDS-R consists of nine questions including ge, orienttion in time, orienttion in plce, repeting three words, seril 7 s, ckwrd digit spn, reclling three words, reclling five ojects, generting nmes of vegetles, covering orienttion, memory, ttention, clcultion, nd verl fluency. Compred with MMSE, the reltive weight of the mesures for memory ws strengthened nd the mesure for lnguge ws dded. In the MMSE, memory testing is limited to rief, delyed recll of three words, nd the items for reding nd writing re sent in the Koren version. Since these strengthened or dded mesures re exmining the cognitive domins usully impired erly in AD [16, 17], they my hve improved the dignostic ccurcy of the HDS-R for AD. Since the MMSE showed higher flse positive rte in eductionlly disdvntged popultions [14], the difference of the dignostic ccurcy etween the MMSE nd the HDS-R my e igger in the low-educted sujects. However, the HDS-R showed higher ccurcy in the higheduction group (z = 2.94, p = 0.002) s well s in the low-eduction group (z = 2.23, p = 0.013) in the present study indicting tht the superiority of the HDS-R to the MMSE in dignosing AD my not e influenced y the eductionl level of sujects. This further supports tht the superiority of the HDS-R to the MMSE in dignosing AD my e ttriuted to the differences in the cognitive mesures included in the two tests. Mny previous studies included prticipnts with severe AD, nd thus few studies hve provided informtion on the ccurcy of screening tests for detecting mild AD. The evidences on dignostic ccurcy from those studies my e most ppropritely extrpolted to detection of moderte AD. Although the HDS-R ws more ccurte thn the MMSE in dignosing mild AD, the AUC of ech test for mild AD ws lower thn tht for whole AD, indicting tht it my e influenced y the severity of AD. Thus it would e etter to confine the sujects to mild cses, who re the focus of screening tests in evluting screening tests. In conclusion, lthough oth the MMSE nd HDS-R re useful screening tests for AD, the HDS-R is etter thn the MMSE in the spect of dignostic ccurcy for AD regrdless of the eductionl level of the sujects. Acknowledgment This work ws supported y the Biotech 2000 (Grnt No. 98- N A-12) of the Ministry of Science nd Technology of Kore. Dignostic Accurcy for AD of MMSE nd HDS-R Dement Geritr Cogn Disord 2005;19:
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Original Research Article. Dement Geriatr Cogn Disord 2007;24: DOI: /
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