E L S E V I E R Archives of Gerontology and Geriatrics

21 (1995) 27-34

ARCHIVES OF GERONTOLOGY AND GERIATRICS

Disturbed visuo-spatial orientation in the early stage of Alzheimer's dementia

J~inos K~ilmfin*, Erzs6bet Magl6czky, Zolt~in Janka

Szent.Gy#rgyi University Medical School, Semmelweis u. 6., H-6725 Szeged, Hungary

Received 16 September 1994; revision received 21 October 1994; accepted 30 March 1995

Abstract

A pilot study was conducted to assess previously unrecognized visuo-spatial disturbances in 45 Alzheimer's demented (AD) patients and 59 control persons all over the age of 65 years, living in the community. The results of the Clock Drawing Test (CDT) revealed high frequen- cy (78%) of deficient performative visuo-spatial skills of mild and moderate demented AD patients. The severity of dementia was found to be a good predictor of the deficit in visuo- constructive performance. The most frequent drawing mistakes were the misplacement of numbers and clock hands, which may relate to dysfunctions of the right inferior parietal cor- tex. The right-left orientation (RLO) for the own body was not deteriorated in AD patients. However, significantly lower scores for RLO in the mental rotation subtest were found in mild and moderate AD groups. There were large inter-individual differences in the test scores of both demented groups. Thirty-one percent and 49% of the AD patients scored 0 points or within the normal range (more than 4 points), respectively, indicating a pseudofocal onset pat- tern of the dementia. The results of the CDT and Right-Left Orientation Test (RLOT) with mental rotation showed significant positive correlation with other cognitive functions of Mini Mental State Exam, such as attention-calculation, recall and writing, and indicate that the visuo-spatial orientation (VSO) is a composite of different cognitive skills. The CDT and RLOT appears to be a useful tool for screening the elderly for disturbed VSO.

Keywords: Visuo-spatial orientation; Clock Drawing Test; Right-Left Orientation Test; Mental rotation; Alzheimer's dementia

* Corresponding author.

0167-4943/95/$09.50 © 1995 Elsevier Science Ireland Ltd. All rights reserved SSDI 0167-4943(9 5)00639-3

28 J. K~ilm(m et al./ Arch. Gerontol. Geriatr. 21 (1995) 27-34

1. Introduction

The disturbance of visuo-spatial orientation (VSO) is considered to be the second most frequent cognitive sign of dementia affecting nearly every function of life (Wilson et al., 1982; Moore and Wyke, 1984; Liu et al., 1991; Almkvist and Backman, 1993). The symptoms of VSO can manifest as disturbances of dressing, misplacing objects, wandering, getting lost, traffic accidents, driving problems (De Leon et al., 1984; Buncher and Larson, 1987; Friedland et al., 1988; Lucal-Blaustein et al., 1988) so their early recognition is considered to be very important for both the demented person and the relatives.

From a neuropsychiatric point of view different deficits of VSO can be separated such as disturbances of extrapersonal and personal orientation, fight-left orientation (RLO) and mental rotation (Raskin et al., 1992), all of them with perceptual, cogni- tive and functional components.

Despite their importance, relatively little is known about the nature and preva- lence of different VSO disturbances in early stages of Alzheimer's dementia (AD). Disturbed visuo-constructive functions were observed on AD subjects by Henderson et al. (1989). Cogan (1985) and Kaszniak et al. (1978) reported deficient right-left discrimination of AD patients. On the other hand Fischer et al. (1990) found disturb- ed RLO only on confronting the patients with the objects. However, intact spatial rotation skills of AD patients were described by others (Flicker et al., 1988; Brouwers et al., 1984).

The main purpose of this study was 3-fold: (1) to determine the frequency of visuo- constructive and RLO disturbances in persons in early stages of AD; (2) to provide more information about the nature of RLO deficit: whether the egocentric or the mental rotation component is more disturbed? (3) to determine the relationship between the disturbances of VSO and other cognitive functions.

To answer these questions we used 2 different types of test. The Clock Drawing Test (CDT) was originally used to assess constructional apraxia by neurologists (Crickley, 1953). Later several other studies employed it as a rapid screening method in AD (Sunderland et al., 1989; Wolf-Klein et al., 1989; Dastoor et al., 1991; Shulman et al., 1986, 1993). The Right-Left Orientation Test (RLOT) is a part of the Benton test (Benton et al., 1983), modified by Fischer et al. (1990) to assess RLO in personal and extrapersonal space.

2. Subjects and methods

2.1. Subjects A total number of 104 volunteers participated in the study. The 59 control and

45 AD subjects were all over the age of 65 years. They were recruited from 5 day-care centers for the elderly in Szeged city, Hungary. Those who had a history of cerebrovascular accidents, seizure disorder, severe hypertension, diabetes mellitus, visual deficits, physical disabilities or severe tremor were excluded from further eval- uation. The demented persons fulfilled the NINCDS-ADRDA criteria of probable AD (McKhann et al., 1984) and DSM-III-R criteria for primary degenerative

J. KAim~n et al./ Arch. Gerontol. Geriatr. 21 (1995) 27-34 29

dementia of Alzheimer's type (APA, 1987). The subjects' characteristics are presented in Table 1. All subjects were informed about the nature of the study and had signed a written consent. The protocol was approved by the ethical committee of the Albert Szent-Gy6rgyi Medical University, Szeged. All persons participating in the study were free of psychotropic medication and according to the primary caregivers' opinion none of them had serious problems in their daily functioning.

2.2. Tests and procedures

First the Mini Mental State Exam (MMSE) (Folstein et al., 1975) was admin- istered to the participants. Subsequently the CDT was performed according to the procedure of Sunderland et al. (1989). In brief, a predrawn circle was presented and the proband was asked 'to draw a clock'. The same instruction was repeated in case the subjects had any questions. Later he or she was asked 'to draw in the hands of the clock to show 2:45'. Finally the RLOT was performed (Benton et al., 1983, modi- fied according to Fischer et al., 1990). As a pretest a 40-cm high doll was held in front of the proband and he or she was asked to show the doll's: (1) one eye, (2) one ear, (3) one hand, (4) one shoulder, (5) the belly, (6) one knee. If any of the answers were incorrect we did not ask any further questions. If all the answers were correct, we asked the person to show his or her own: (1) left hand, (2) right eye, (3) left ear, (4) right shoulder, (5) right hand and (6) left knee. Subsequently the proband was asked to show the confronting doll's: (1) left ear, (2) right shoulder, (3) left knee, (4) right eye, (5) left hand, (6) right ear.

2.3. Evaluation

The subjects were grouped into control and dementia groups according to their MMSE scores, 27-30 points and 0-23 points, respectively. The dementia group was further divided into mild (MMSE score: 19-23) and moderate (MMSE score: 10-18) subgroups. The CDT was scored from 1-10 points according to Sunderland et al.

Table I Subject characteristics

Control Mild dementia Moderate dementia

Number of subjects 59 29 16 Age 78.9 4- 7.55 80.0 4- 7.50 79.1 ± 9.20 Sex (F/M) 45/14 19/10 13/3 Education (basic/high school) 40/19 19/10 12/4 MMSE score (points) 28.3 4- 1.07 21.2 4- 1.53" 14.6 ± 2.00**

Values are mean 4- S.D. *Kruskal-Wallis test, t= 86.918, P < 0.001 and Mann-Whitney test with Bonferroni correction, z = -7.68; P < 0.001. **Kruskal-Wallis test, t= 86.918 P < 0.001 and Mann-Whitney test with Bonferroni correction, z =-6.21; P < 0.001.

30 J. /Gi/m6n et al./Arch. Gerontol. Geriatr. 21 (1995) 27-34

Table 2 Scores of CDT and RLOT in relation to mental status

Control Mild demented Moderate (n = 59) (n = 29) demented

(n = 16)

CDT 9.1 4- 1.27 5.4 4- 2.51" 2.9 q- 1.87" RLOT, own body 6.0 ~- 0.00 5.9 4- 0.26 5.6 4- 1.09

RLOT, doll 5.2 4- 1.61 3.4 ± 2.71"* 3.3 4- 2.47**

Values are mean ± S.D. *Kruskal-Wallis test, P < 0.001 and Mann-Whitney test with Bonferroni correction, P < 0.001.

**KruskaI-Wallis test, P < 0.001 and Mann-Whitney test with Bonferroni correction, P < 0,005.

(1989). The RLO tests were scored from 0 to a maximum of 6 points (each correct answer was 1 point).

2.4. Statistical methods Data presented are mean ~- S.D. unless otherwise specified. All test statistics

considered to be significant at P < 0.05 or better. The differences between the groups and within the subgroups were calculated using non-parametric Mann- Whitney test and Kruskal-Wallis test with Bonferroni adjustment for multiple comparisons. Pearson correlation coefficients were used to examine the relationship between scores of MMSE and CDT or RLOT. The significance of the frequency dis- tributions were calculated by Fischer test (Monte Carlo method). The inter-rater re- liability of CDT was calculated by Spearman rank correlation and weighted kappa statistics. The Statgraphics Statistical Graphic System (copyright 1985-88, Educa- tional Institution Edition, Version 3, Rockford, Maryland), StatXact (1989, 1991 Cytel Software Corporation, Cambridge, MA) and STATA 1992 (Computing Resource Center, Santa Monica, CA) software were used for the different statistical calculations.

Table 3 Collapsed CDT scores in relation to mental status

Control Demented

Mild Moderate Total

Score (points) N % N % N % N %

< 8 5 8.5 20 69 15 93.7 35 78 >8 54 91.5 9 31 1 6.3 10 22

Fischer test (Monte Carlo method) 99% confidence interval, P < 0.001.

J. KdlmtJn et al. / Arch. Gerontol. Geriatr. 21 (1995) 27-34

Table 4 Collapsed RLOT doll scores in relation to mental status

31

Control Demented

Mild Moderate Total

Score (points) N % N % N % N %

<5 8 13.6 14 48.3 9 56.3 23 51 :~5 51 86.4 15 51.7 7 43.7 22 49

Fischer test (Monte Carlo method) 99e confidence level, P < 0.01.

3. Results

Table 2 presents means and S.D. of CDT and RLOT. Both dementia groups scored significantly lower in CDT than the control group. The most frequent errors were misplacement of numbers and clock hands but errors in the sequence of numbers, misplacements, omissions, perseverations were also very common. The mean scores of RLOT own body were slightly lower than that of the control group but these differences were not statistically significant. The Mann-Whitney test with Bonferroni correction identified differences between the control and mild and moderate dementia groups in the RLOT with doll, but the differences did not dis- criminate the two dementia groups from each other.

The collapsed distributions of CDT error scores for the different groups are shown in Table 3. If we select score 8 as an arbitrary cut-off value, the specificity and sensi- tivity of the test were 92 and 78%, respectively. Table 4 presents distribution of RLOT with doll scores in relation to mental status. There were persons with 0 scores

Table 5 Distribution of RLOT doll scores in relation to mental status

Control Demented

Mild Moderate Total

Score (points) N % N % N % N %

0 2 3 10 35 4 25 14 31 1 3 5 0 0 0 0 0 0 2 I 2 0 0 3 19 3 7 3 1 2 3 10 1 6 4 9 4 1 2 I 3 1 6 2 4 5 10 17 3 10 2 13 5 11 6 41 70 12 41 5 31 17 38

Fischer test (Monte Carlo method) 99°6 confidence level, P < 0.001.

32 J. Kd/mdn et al. / Arch. Gerontol. Geriatr. 21 (1995) 27-34

Table 6 Correlation of different items of MMSE with the scores of CDT and the doll RLOT

CDT Doli/RLOT

MMT item Corr. coeff. P Corr. coeff. P

Orientation 0.5050 < 0.001 0.3079 < 0.002 Registration 0.1740 > 0.05 0.1222 < 0.2 Attention/calculation 0.6764 < 0.001 0.5107 < 0.001 Recall 0.6002 <0.001 0.3337 <0.001 Naming 0.1236 >0.15 I <0.001 Repetition 0.4086 < 0.001 0.2345 < 0.02 Three-stage command 0.3448 <0.01 0.1596 <0.1 Reading 0. 5446 < 0.001 0.3413 < 0.001 Writing 0.5945 < 0.001 0.3966 < 0.001 Copying 0.5281 < 0.001 0.2082 < 0.03 Total score 0.7424 < 0.001 0.4284 < 0.001

in each group and this number was relatively high in the mild dementia group (10 persons). The collapsed RLOT doll scores (Table 5) indicate that 48 and 56% of mild and moderate demented persons, respectively, scored less than 5 points. The total scores of CDT show significant positive correlation with the attention- calculation, recall and writing items of MMSE (Table 6). Significant but smaller cor- relations were found with the same items with the total scores of the doll part of RLOT.

4. Disemsion

The results of CDT suggest high frequency (78%) of deficient visuo-constructive performance in the early stage of AD. These findings confirm the results of Wolf-Klein et al. (1989), Dastoor et al. (1991), Toukko et al. (1992) and Shulman et al. (1993). The most frequent drawing errors: arrangement problems, misplace- ments, omissions, pcrseverations, were similar to those found in the spontaneous drawing of AD patients by Moore and Wyke (1984) and reflect early disturbances in the function of the right inferior parietal cortex (De Renzi, 1982). It is important to note that the deficit of the clock drawing performance was found to be present in both dementia groups and the severity of the dementia predicted the degree of disturbance in the visuo-constructive performation. Therefore, the CDT could be a useful fast screening method to determine the existence and severity of AD. In our case the specificity and sensitivity of the CDT were 92 and 78%, respectively, in agreement with the results of Wolf-Klein et al. (1989) and Toukko et al. (1992).

The RLO ability for the own body was not apparently damaged in AD patients. On the other hand, the doll part of the RLOT revealed deficits in the egocentric men- tal rotation capacity of the AD patients, but it was not differentially sensitive to the degree of severity of dementia. The results of this study support the findings of Fischer et al. (1990) and indicate that mild and moderate demented AD patients have

J. l(xilmdn et al. / Arch. Gerontol. Geriatr. 21 (1995) 27-34 33

more impairment in tasks requiring visuo-constructive manipulation and mental ro- tation in the extrapersonal space (CDT, RLOT with doll) than in the personal one (RLOT own body). Others (Flicker et al., 1988) failed to demonstrate any impair- ment in spatial rotation in AD with Money's Standardized Road Map Test (Money et al., 1965). This controversy might be attributed to the different testing methods used in the two studies.

The deterioration of spatial mental rotation skills during the aging process has been observed by several authors (Cerella et al., 1981; Berg et al., 1982; Flicker et al., 1988;). In our study we went further and described the loss of these skills in mild and moderate AD patients. However this deficit was found to be present to a dif- ferent extent in the demented groups. Thirty-five percent and 25% of the mild and moderate AD patients, respectively, scored 0 points, indicating considerable symp- tomatic variability in the early stage of dementia. We suppose that the reason for the great inter-individual differences is that the neurodegenerative process does not affect the brain of different persons in the same way in the early stages of AD, pro- ducing pseudofocal onset pattern in some cases, as revealed by positron-emission tomography studies (Foster et al., 1983; Haxby et al., 1986).

The results of our correlation evaluations show that the disturbances of VSO is strongly related to the global severity of the dementia and other cognitive functions such as attention-calculation, recall, reading and writing and indicate that the VSO is a composite of different cognitive skills.

Because of the frequency and importance of VSO skills in the daily functioning, we consider that a regular testing would be important in high risk population. We suggest the CDT and RLOT as useful tools for this type of screening in AD.

Acknowledgements

The authors gratefully acknowledge the participation of all persons involved in the study and the help of the caregivers from the day-care centers. This study was sup- ported by the grant of Health Scientific Board ETT, T04, 589/1993 (Hungarian Ministry for Welfare).

Rdemnees

Almkvist, O. and Beckman, L. (1993): Progression in Alzheimer's disease: sequencing of neuro- psychological decline. Int. J. C~riatr. Psychiatr., 8, 755-763.

American Psychiatric Association (APA) (1987): Diagnostic and Statistical Manual of Mental Disorders, 3rd Ed. revised. American Psychiatric Association, Washington, D.C.

Benton, A.L., Hamsher, K., Varney, N.R. and Spccn, O. (1983): Contributions to Neuropsychological Assessment. Oxford University Press, New York.

Berg, C., Hertzog, C. and Hunt, E. (1982): Age differences in the speed of mental rotation. Dee. Psychol., 18, 95-107.

Brouwers, P., Cgx, C., Martin, A., Chase, T. and Fcdio, P. (1984): Differential perceptual-spatial impair- ment in Huntington's and Alzheimcr's dementias. Arch. Neurol., 41, 1073-1076.

Buncher, D.M. and Larson, E.B. (1987): Falls and fractures in patients with Aizheimer-type dementia. J. Am. Med. Assoc., 257, 1492-1495.

Ccrclla, J., Poon, L.W. and Fozard, J.L. (1981): Mental rotation and age reconsidered. J. G-erontol., 36, 620-624.

34 J. Ktilmdtn et aL /Arch. Gerontol. Geriatr. 21 (1995) 27-34

Cogan, D.G. (1985): Visual disturbances with focal progressive dementing disease. Am. J. Ophthal., 100, 68-72.

Crickley, M. (1953): The Parietal Lobes. Hafner Publishing Company, Inc., New York. Dastoor, D.P., Schwartz, G. and Kurzman, D. (1991): Clock-drawing - - an assessment technique in

dementia. J. Clin. Exp. Gerontol., 13, 69-85. De Leon, M.J., Potegal, M. and Gurland, B. (1984): Wandering and parietal signs in senile dementia of

Alzheimer's type. Neuropsychology, I i, 155-157. De Renzi, E. (1982): Disorders of Space Exploration and Cognition. Wiley, Chichester. Fischer, P., Marterer, A. and Danielczyk, W. (1990): Right-left disorientation in dementia of the

Alzheimer type. Neurology, 40, 1619-1620. Flicker, C., Ferris, S.H., Crook, T., Reisberg, B. and Bartus, R.T. (1988): Equivalent spatial-rotation

deficits in normal aging and Alzheimer's disease. J. Clin. Exp. Neuropsychol., 10, 387-399. Folstein, M.F., Foistein, S.E. and McHugh, P.R. (1975): Mini-mental state: a practical guide for grading

the cognitive state of patients for the clinician. J. Psychiatr. Res., 12, 189-198. Foster, N.L., Chase, T.N., Fedio, P., Patronas, N.J., Brooks, R.A. and DiChiro, G. (1983): Alzbeimer's

disease: focal changes shown by positron emission tomography. Neurology, 33, 961-965. Friedland, R.P., Koss, E., Kuman, A., Gaine, S., Metzler, D., Haxby, J.V. and Moore, A. (1988): Motor

vehicle crashes in dementia of the Alzheimer type. Ann. Neurol., 24, 782-786. Haxby, J.V., Grady, C.L., Duara, R., Schlageter, N., Berg, G. and Rapoport, S. (1986): Neocortical meta-

bolic abnormalities precede nonmemory cognitive defects in early Alzheimer's-type dementia. Arch. Neurol., 43, 882-885.

Henderson, V.W., Mack, W. and Williams, B.W. (1989): Spatial disorientation in Alzheimer's disease. Arch. Neurol., 46, 391-394.

Kaszniak, A.W., Fox, I., Gandell, D.L., Garron, D.C., Huckmann, M.S. and Ramsey, R.G. (1978): Predictors of mortality in presenile and senile dementia. Ann. Neurol., 3, 246-252.

Liu, L., Gauthier, L. and Gauthier, S. (1991): Spatial disorientation in persons with early dementia of the AIzbeimer type. J. Am. Occup. Therap., 45, 67-75.

LucaI-Blaustein, M.J., Filipp, L., Dungan, C. and Tune, L. (1988): Driving in patients with dementia. J. Am. Geriatr. Soc., 36, 1087-1091.

McKhann, G., Drachman, D., Folstein, M., Katzman, R., Price, D. and Stadlan, E.M. (1984): Clinical diagnosis of Alzheimer's disease: report of the NINCDS ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer',s disease. Neurology, 34, 939-944.

Money, J., Alexander, D. and Walker, H.T. (1965): A Standardized Road-Map Test of Direction Sense. Johns Hopkins University Press, Baltimore.

Moore, V. and Wyke, M.A. 0984): Drawing disability in patients with senile dementia. Psychol. Med., 14, 97-105.

Raskin, S.A., Borod, J.C. and Tweedy, J.R. (1992): Set-shifting and spatial orientation in patients with Parkinson disease. J. Clin. Exp. Neuropsychol., 14, 801-821.

Shulman, K.I., Shedletsky, R. and Silver, I.L. (1986): The challenge of time: clock drawing and cognitive function in the elderly. Int. J. Geriatr. Psychiatr., l, 135-140.

Shulman, K.I., Gold, D.P., Cohen, C.A. and Zucchero, C.A. (1993): Clock drawing and dementia in the community: a longitudinal study. Int. J. Geriatr. Psychiatr., 8, 487-496.

Sunderland, T., Hill, J.L., Mellow, A.M., Lawlor, B.A., Gundersheimer, J., Newhouse, P.A. and Graf- man, J.H. (1989): Clock drawing in Alzheimer disease: a novel measure of dementia severity. J. Am. Geriatr. Soc., 37, 725-729.

Toukko, H., Hadjistavropoulos, T., Miller, A. and Beattie, B.L. (1992): The clock test: a sensitive measure to differentiate normal elderly from those with AIzheimer disease. J. Am. Geriatr. Soc., 40, 579-584.

Wilson, R.S., Kaszniak, A.W., Bacon, L.D., Fox, J.H. and Kelly, M.P. (1982): Facial recognition memory in dementia. Cortex, 18, 329-336.

Wolf-Klein, G.P., Silverstone, F.A., Levy, A.P. and Brod, M.S. (1989): Screening for Alzheimer's disease by clock drawing. J. Am. Geriatr. Soc., 37, 730-734.