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The pattern of reading deterioration in dementia of the Alzheimer type: Observations and implications
BRAIN
AND
LANGUAGE
29, 315-323 (1986)
The Pattern of Reading Deterioration in Dementia of the Alzheimer Type: Observations and Implications JEFFREY
L. CUMMINGS
Nerrrobehavior Unit. West Los Angeles VAMC (Brentwood DiGsion), und Deptrrtmenf of Neurolog.v, UCLA S~~hool of Medkine
JOHN Psychologv
Senlice.
P. HOULIHAN
West Los Angeles VAMC, und Deportment UCLA School of Medicine
of P.c~c~hology,
AND MARY ANN HILL Reseurch und Development Service, West Los Angeles VAMC (Brentuwod the Depurtment of Psychiutty und Biobehoviorul Science, UCL,A School of Medicine
Division),
and
Thirteen patients with dementia of the Alzheimer type (DAT) were tested for their ability to read aloud and to read with comprehension. Reading aloud was preserved in all but the most severely impaired cases and was found to be relatively independent of intellectual deterioration. Reading comprehension declined progressively with increasing dementia severity and correlated well with quantitative mental status assessments. The results suggest that the pattern of reading deterioration may aid in the clinical identification of DAT, that the disturbance of reading comprehension is a linguistic deficit rather than a product of visualperceptual disturbances, and that the alexia is more consistent with an instrumental loss than a de-developmental model of dementia. 0 1986 Academx Press, 1~.
This research was supported by the Veterans Administration, the Los Angeles Chapter of the Alzheimer’s Disease and Related Disorders Association, and the John Douglas French Foundation. The authors are indebted to Dr. Robert Neshkes and Dr. Stephen Read for allowing us to study their patients. Ms. Norene Hiekel and Ms. Vernie White prepared the manuscript. Dr. Houhhan is currently at the Psychology Service, VAMC Portland, Oregon. Address reprint requests to Jeffrey L. Cummings, M. D., West Los Angeles VAMC (Brentwood Division), Neurobehavior Unit, Ward 256b (69l/Bll l), 11301 Wilshire Boulevard, Los Angeles, CA 90073. 315 0093-934X/86 $3.OO Copyright 0 1986 by Academic Press, Inc. All rights of reproduction in any form reserved.
316
CUMMINGS,
HOULIHAN,
AND HILL
Dementia of the Alzheimer type (DAT) has been shown to produce a specific pattern of spoken verbal output resembling transcortical sensory aphasia and characterized by fluent verbalization, impaired comprehension, anomia, and preserved repetition (Schwartz, Marin, & Saffron, 1979; Appell, Kurtesz, & Fisman, 1982; Cummings, Benson, Hill, & Read, 1985). The reading abilities of DAT patients have been studied less exhaustively, but preliminary investigations have revealed that a dissociation of reading aloud and reading comprehension is common, with relative preservation of the ability to read aloud even when reading comprehension is severely compromised (Schwartz et al., 1979; Benson, Cummings, & Tsai, 1982; Cummings & Benson, 1983; Obler & Albert, 1984; Cummings et al., 1985). In a detailed case study, Schwartz and colleagues (1979) reported that their patient could apply grapheme-to-phoneme correspondence rules for nonwords and non-English words and correctly read English words with irregular spellings. Sevush (1984) described similar findings in a larger group of patients. Such abilities have not been explored in other DAT patients or related to the severity of intellectual decline in DAT. Further characterization of the reading abilities of DAT patients is of interest for several reasons. First, detailed analysis of reading in DAT may’ establish features that aid in distinguishing DAT from other dementing illnesses and that help identify the stage of advancement of the DAT. Second, the pattern of reading deterioration may help determine if reading comprehension deficits are based on perceptual deficits produced by disturbances at the visual-analytic level or are semantic comprehension deficits secondary to linguistic deterioration. Third, the reading characteristics may aid in deciding between two prevalent models of DAT: (1) dementia is a product of instrumental failures similar to the infarctioninduced aphasias, or (2) cognitive decline is a dedevelopmental process with a progressive de-differentiation of language skills. To help clarify these questions, a series of reading tasks was chosen and administered to DAT patients. SUBJECTS
The subjects consisted of 13 patients with DAT. They were 61 to 82 years old and all but one were right-handed. All had at least an eighthgrade education (range 8-16 years), and none of the reading tests (except the New Adult Reading Test as explained below) required reading skills beyond the elementary school level. All patients had vision adequate to allow unimpaired perception of the written stimuli. All subjects met Diagnostic and Statistical Manual of Mental Disorders (1980) criteria for primary degenerative dementia and National Institute of Neurologic and Communicative Disorders and Stroke criteria for probable DAT (Mckhann et al., 1984). None of the patients suffered from an active
READING
DETERIORATION
IN DEMENTIA
317
systemic illness or had evidence of an affective disorder, and all had a Hachinski Ischemia Scale score of 4 or less, consistent with degenerative dementia (Hachinski et al., 1975). The severity of dementia was assessed with the Mini-Mental State Examination (MMSE) (Folstein, Folstein, & McHugh, 1975), and a score of 24/40 or less was required for entry into the study. MMSE scores ranged from 1 to 19 (mean 10.0). READING TESTS AND RESULTS
Table 1 presents a summary of the reading test results. The tests and the group and individual response characteristics are described below. Tests of Reading Aloud Letter reading. The most elementary visual stimuli presented were letters. Each patient was asked to read aloud 30 randomly chosen letters: 10 uncomplicated letters, 10 incomplete letters, and 10 letters partially obscured by multiple diagonal lines. This skill was remarkably resistant to disruption by the dementia. Patients with MMSE scores of 5 or more read from 27 to 30 of the letters. Dividing the ordered sample into median (half the values fell below and half above), first quartile (Q, ; 25% below, 75% above), and third quartile (Q3-; 75% below, 25% above), the scores ranged only from 29 (Q3-) to 27.5 (Q,), and 11 of 13 patients scored above Q,. Two severely immpaired patients with MMSE scores of 4 and 1 correctly identified 20 and 24 of 30, respectively. Incomplete and obscured letters were read as easily as the uncomplicated presentation. Word reading. Each patient was asked to read aloud 30 high-frequency four-letter words and 10 prepositions. The 20 words consisted of 10 “emotional” words (e.g., kill, pain, rape), 10 concrete words (e.g., boat, suit, plug), and 10 abstract words (e.g., time, form, unit) matched for word frequency (Landis, Graves, Benson, & Hebben, 1983).Word reading ability was preserved in all but the most impaired patients. Eleven of the patients were able to read 38/40 words. The sample ranged from 38 (Q,) to 40 (Q-0 and only 2 of 13 patients scored below Q,. Only 2 patients had scores deviating markedly from 40 and they had MMSE scores of 6 and 1, respectively. A severely impaired patient with an MMSE of 4 performed the task perfectly. Reading obscured words. This word reading test was designed to help separate perceptual from linguistic deficits. Ten partially obscured words (words with several diagonal lines drawn through them) were presented. Such stimuli exaggerate the visual-perceptual deficits of patients with visual agnosia (Landis et al., 1982) but have little effect on the reading of DAT patients. Ten of the 13 patients read 9-lO/lO words, 3 patients with MMSE scores of 7, 6, and 1 read 4, 7, and O/10, respectively. The quartiles of the sample ranged from 8 (Q1) to 10 (QX), and 11 of 13 patients scored above Q,.
6
5
5
10
6
6
67
9
10
67
29 40
30 30
16
19
2
74
1
73
4
5
5
1
2
62
6
10
29 40
13
82
44
6
10
27 40
15
78
3
8
5
74
6
10
29 40
13
5 78
TEST INFORMATION
Note. Q,, quartile 1; M, median; Q,, quartile 3.
Reading comprehension Word vs. nonword recognition Following written commands Sentence comprehension
Reading aloud Letter reading Word Reading Reading obscured words Commands
Age: MMSE:
Patient information and tests
READING
TABLE I
6
4
78
6
10
29 38
12
6 74
4
6
65
6
10
29 40
10
7 JO
Patient
3
4
53
6
10
28 40
8
8 78
0
2
55
2
4
28 38
7
61
9
0
1
45
6
29 25 7
10 74 6
FROM 13 PATIENTS WITH DEMENTIA
5
2
62
6
10
28 39
76 5
11
3
0
52
6
20 40 9
78 4
12
0
0
47
0
24 0 0
1
77
13
OF THE ALZHEIMER
1
1
50
6
27.5 38 8
5.5
QI
TYPE
4
4
62
6
10
29 40
10
M
5.5
5
67
6
10
29 40
14
Q,
10
6
80
6
10
30 40
30
Best possible score
READING
DETERIORATION
IN DEMENTIA
319
Commands. Written commands from the Western Aphasia Battery (WAB) (Kertesz, 1979) were administered to all patients. Reading the commands aloud was performed perfectly by all except two of the subjects and these had MMSE scores of 7 and 1. Reading Comprehension Word vs. nonword recognition. In this test, each patient was shown 80 four-letter combinations. Using the method described by Patterson (1979), half the stimuli were English words and half were nonsense letter arrangements. The patient read the words aloud and indicated the nonword nature of the nonsense letter combinations. On this task, word discrimination skills were present to a limited extent even in the most deteriorated patient, but the discrimination ability declined as the dementia worsened in severity (correlation with MMSE: r = 5.02, p < .05). Understanding written commands. Comprehension of commands from the WAB was impaired, and there was a significant correlation with increasing severity of intellectual impairment (correlation with MMSE, r = .701, p < .005). Nine of the 13 patients could read aloud more commands than they could read with comprehension; in no case was the reverse pattern found. There was a significant difference between the ability of the patients to read commands aloud and their ability to comprehend what they read (t = 3.438, p < .005). Understanding sentences. Sentence comprehension was tested using sentences from the Boston Diagnostic Aphasia Examination (Goodglass & Kaplan, 1983). A perfect score of lO/lO was obtained by the least impaired DAT patient, but sentence comprehension declined steadily with advancing dementia (correlation with MMSE scores, r = .699, p < .005). New Adult Reading
Test
The New Adult Reading Test (NART) (Nelson & O’Connell, 1978) consists of 50 irregular words (e.g., psalm, heir, facade) that can be pronounced correctly only if the patient is familiar with them: they do not obey the usual grapheme-to-phoneme conversion rules. Performance on this task was more variable than on any other. Scores ranged from 39 to 0 with a mean of 17.2 (median 19.5). Inspection of the distribution of scores revealed no relation between test performance and dementia severity. When performing the test, patients either read the word correctly or failed to produce a response. Errors related to phonetic reading were not observed. DISCUSSION
The DAT patients in this study showed a consistent pattern of reading impairment. Reading letters and words aloud, reading partially obscured
320
CUMMINGS,
HOULIHAN,
AND HILL
letters and words, reading irregular words and reading commands aloud, although failed by patients in the most advanced stages of dementia, were relatively preserved through most of the range of intellectual impairment and showed little association with declining MMSE scores. Reading comprehension, however, demonstrated no such selective sparing and all tests involving understanding of written material (distinguishing words from nonsense letter arrangements, performance of written commands, and sentence comprehension) all declined systematically with advancing dementia and correlated significantly with decreasing MMSE scores. The observations made in this study confirm and extend those made by previous investigators. In a case report, Schwartz et al. (1979) showed that their DAT patient could read nonwords and non-English words using appropriate English phonological rules; she could also read irregular English words correctly. Reading comprehension was not extensively studied, but the patient was partially successful in written word-picture matching. Studies of groups of carefully diagnosed DAT patients by Appell et al. (1982) and Cummings et al. (1985) found a dissociation between the ability to read aloud and reading comprehension. Reading both words and sentences aloud was preserved, whereas comprehension of written words, commands, and sentenceswas characteristically impaired. Sevush (1984) found a similar dissociation and concluded that the predominant reading defect in DAT was one of semantic processing. Thus, studies addressing this issue have consistently demonstrated that DAT patients are able to phonologically encode written verbal stimuli but have difficulty semantically decoding such material. Nelson and O’Connell (1978) capitalized on the preserved ability of dementia patients to read irregular words in constructing the NART. They found that this capacity was not significantly affected by the severity of intellectual impairment, and the patients’ ability to read aloud could thus be used to assess the size of their premorbid vocabulary and to estimate their premorbid intellectual level. The research subjects, however, were not limited to DAT and consisted of all subjects with atrophy on computerized tomograms of the head. In the study reported here, a more homogeneous group of clinically diagnosed DAT patients also showed relative preservation of reading irregular words of the NART, and the results support a lack of correlation between dementia severity and this reading ability. Demonstration of the consistency with which a distinction between reading aloud and reading comprehension occurs in DAT suggests that this pattern may be diagnostically useful. Clinical diagnosis of DAT has previously been subject to error rates of at least 18 to 30% (Ron, Toone, Garralda, & Lishman, 1979; Sulkava, Haltia, Paetau, Wikstrom, & Palo, 1983), and attention to the pattern of alterations occurring in spoken language and reading of dementia patients may help distinguish DAT
READING
DETERIORATION
IN DEMENTIA
321
from other causes of acquired intellectual impairment (Cummings & Benson, 1983; Cummings et al., 1985). In angular gyrus syndrome, a condition that may closely resemble DAT, for example, Benson et al. (1982) showed that reading aloud and reading comprehension were comparably impaired, and this contrasting pattern aided in distinguishing the syndrome from DAT. The dissociation of reading skills noted in the patients reported here correlates with the distribution of pathologic changes present in DAT. DAT produces its major neuropathological, neurochemical, and metabolic changes on the posterior regions of the cerebral hemispheres in the area of the temporoparieto-occipital junction region (Brun & Gustafson, 1978; Davies, 1978; Benson et al., 1983; Cummings & Benson, 1983; Chase et al., 1984). Focal brain insults in this area are known to dissociate the ability to read aloud and the ability to read with comprehension in the syndrome of transcortical sensory aphasia (Albert, Goodglass, Helm, Rubens, & Alexander, 1981). Thus, the pattern of deterioration of reading skills observed in DAT is a product of the geography of hemispheric involvement and can be used clinically to aid in the identification of the distribution of pathologic alterations characteristic of DAT. The results of this study also help to clarify the question of whether the difficulties experienced by the DAT patient are perceptual or linguistic in nature. Rochford (1971) proposed that the naming deficits exhibited by DAT patients were largely attributable to an impairment of visual recognition, and agnosia is frequently reported as a prominent symptom in DAT. The ability to read aloud, however, is a perceptual task and is preserved in DAT. Moreover, partial obscuration of words, a procedure that increases the reading difficulties of patients with visual agnosia (Landis et al., 1982), did not significantly affect the ability of DAT patients to read aloud. Throughout most of the course of DAT, perceptual disturbances play little role in the patient’s reading comprehension deficits, and the comprehension disturbance appears to reflect a deficit at the semantic decoding level. Patients in more advanced stages of DAT than those studied here may develop perceptual deficits that contribute to the eventual loss of the ability to read aloud. The most severely involved patient in the series (MMSE = 1) exhibited impairment in both reading aloud and reading comprehension, and the former may reflect a late occurring visual processing disturbance. Finally, the observations in this study bear on the central question of the nature of the intellectual impairment in DAT. It has been proposed that the mental deterioration of DAT is a progressive de-development toward a prelinguistic state in which all adult knowledge has been forgotten (Cherkin & Flood, 1983). Others have suggested that the cognitive abnormalities in DAT are best viewed as instrumental deficits similar to those occurring with focal cerebral cortical insults (Cummings & Benson,
322
CUMMINGS,
HOULIHAN,
AND HILL
1983; Cummings, in press), As noted above, the linguistic syndrome exhibited by patients with DAT resembles transcortical sensory aphasia and is similar to that manifested by patients with insults in the posterior aspect of the left hemisphere (Albert et al., 1981). The reading pattern is dissimilar to that exhibited by children learning to read. The lack of correlation between severity of dementia and reading of irregular words on the NART is particularly important in this regard. In the process of reading acquisition, children make grapheme-to-phoneme conversions that lead to mispronunciation of irregular words. The DAT patients did not make such errors and performed better on the test than a de-developmental model would predict. Thus, the results of this study are most consistent with the view that the reading disability and, presumably, the other intellectual abnormalities in DAT are instrumental deficits produced by dysfunction of cortical areas crucial to specific intellectual skills. REFERENCES Albert, M. L., Goodglass, H., Helm, N. A., Rubens, A. B., & Alexander, M. P. 1981. Cinical aspects of dysphasia. New York: Springer-Verlag. Appell, J., Kertesz, A., & Fisman, M. 1982. A study of language functioning in Alzheimer patients. Brain and Language, 17, 73-91. Benson, D. F., Cummings, J. L., & Tsai, S. Y. 1982. Angular gyrus syndrome simulating Alzheimer’s disease. Archives of Neurology, 39, 616-620. Benson, D. F., Kuhl, D. E., Hawkins, R. A., Phelps, M. E., Cummings, J. L., & Tsai, S.Y. 1983. The fluorodeoxyglucose “F scan in Alzheimer’s disease and multi-infarct dementia. Archives of Neurology, 40, 711-714. Brun, A., & Gustafson, L. 1978. Limbic lobe involvement in presenile dementia. Archiv fur Psychiatric
und Nervenkrankheiten,
226, 79-93.
Chase, T. N., Fedio, P., Foster, N. L., Brooks, R., DiChiro, G., & Mansi, L. 1984. Wechsler Adult Intelligence Scale performance. Cortical localization by fluorodeoxyglucose F” positron emission tomography. Archives of Neurology, 41, 1244-1247. Cherkin, A., & Flood, J. F. 1983. In A. Cherkin (Ed.), Intervention in the aging process. New York: Alan R. Liss, Inc. Pp. 225-245. Cummings, J. L. Dementia of the Alzheimer type: challenges of definition and clinical diagnosis. In H. Whitaker (Ed.), Studies in neuropsychology (Vol. 1). In press. Cummings, J. L., & Benson, D. F. 1983.Dementia: a clinicalapproach. Boston: Butterworths. Cummings, J. L., Benson, D. F., Hill, M. A., & Read, S. 1985. Aphasia in dementia of the Alzheimer type. Neurology, 35, 394-397. Davies, P. 1978. Studies on the neurohemistry of central cholinergic systems in Alzheimer’s disease. In R. Katzman, R. D. Terry, & K. L. Bick (Eds.), Alzheimer’s disease: Senile dementia and related disorders. New York: Raven Press. Pp. 453-468. Diagnostic and statistical manual of mental disorders, 1980. Washington, DC: American Psychiatric Association. 3rd ed. Folstein, M. F., Folstein, S. E., & McHugh, P. R. 1975. Mini-mental state. Journal of Psychiatric Research, 12, 189-198. Goodglass, H., & Kaplan, E. 1983. Boston Diagnotic Aphasia Examination. Philadelphia: Lea & Febiger.
READING DETERIORATION
IN DEMENTIA
323
Hachinski, V. C., Iliff, L. D., Zilka, E., Du Boulay, G. H., McAllister, V. L., Marshall, J., Russell, R. W. R., & Symon, L. 1975. Cerebral blood flow in dementia. Archives of Neurology, 32, 632-637. Kertesz, A. 1979. Aphasia and associated disorders: Taxonomy, localization, and recovery. New York: Grune & Stratton. Landis, T., Graves, R., Benson, D. F., & Hebben, N. 1982. Visual recognition through kinaesthetic mediation. Psychological Medicine, 12, 515-531. Landis, T., Regard, M., Graves, R., & Goodglass, H. 1983. Semantic paralexia: A release 21, of right hemispheric function from left hemispheric control? Neuropsychologia, 359-364. McKhann, G., Drachman, D., Folstein, M., Katzman. R., Price, D., & Stadlan, E. M. 1984. Clinical diagnosis of Alzheimer’s disease: Reprt of the NINCDS-ADRDA work group under the auspices of the Department of Health and Human Service task force on Alzheimer’s disease. Neurology, 34, 939-944. Nelson, H. E., & O’Connell, A. 1978. Dementia: The estimation of premorbid intelligence using the New Adult Reading Test. Cortex, 14, 234-244. Obler, L. K, & Albert, M. C. 1984. Language is aging. In M. L. Albert (Ed.), Clinical neurology of aging. New York: Oxford Univ. Press. Pp. 245-253. Patterson, K. E. 1979. What is right with “deep” dyslexic patients? Brain and Language, 8, 111-129. Rochford, G. 1971. A study of naming errors in dysphasic and demented patients. Neuropsychologia,
9, 437-443.
Ron, M. A., Toone, B. K., Garralda, M. E., & Lishman, W. A. 1979. Diagnostic accuracy in presenile dementia. British Journal of Psychiatry, 134, 161-168. Schwartz, M. F., Marin, 0. S. M., & Saffron, E. M. 1979. Dissociations of language function in dementia: A case study. Brain and Language, 7, 277-306. Sevush, S. 1984. Oral versus semantic reading in Alzheimer’s disease. Neurology 34(Suppl. 1), 102 (abstract). Sulkava, R., Haltia, M., Paetau, A., Wikstrom, J., & Palo, J. 1983. Accuracy of clinical diagnosis in primary degenerative dementia: Correlation with neuropathological findings. Journal
of Neurology,
Neurosurgery,
and Psychiatry,
46, 9-13.
AND
LANGUAGE
29, 315-323 (1986)
The Pattern of Reading Deterioration in Dementia of the Alzheimer Type: Observations and Implications JEFFREY
L. CUMMINGS
Nerrrobehavior Unit. West Los Angeles VAMC (Brentwood DiGsion), und Deptrrtmenf of Neurolog.v, UCLA S~~hool of Medkine
JOHN Psychologv
Senlice.
P. HOULIHAN
West Los Angeles VAMC, und Deportment UCLA School of Medicine
of P.c~c~hology,
AND MARY ANN HILL Reseurch und Development Service, West Los Angeles VAMC (Brentuwod the Depurtment of Psychiutty und Biobehoviorul Science, UCL,A School of Medicine
Division),
and
Thirteen patients with dementia of the Alzheimer type (DAT) were tested for their ability to read aloud and to read with comprehension. Reading aloud was preserved in all but the most severely impaired cases and was found to be relatively independent of intellectual deterioration. Reading comprehension declined progressively with increasing dementia severity and correlated well with quantitative mental status assessments. The results suggest that the pattern of reading deterioration may aid in the clinical identification of DAT, that the disturbance of reading comprehension is a linguistic deficit rather than a product of visualperceptual disturbances, and that the alexia is more consistent with an instrumental loss than a de-developmental model of dementia. 0 1986 Academx Press, 1~.
This research was supported by the Veterans Administration, the Los Angeles Chapter of the Alzheimer’s Disease and Related Disorders Association, and the John Douglas French Foundation. The authors are indebted to Dr. Robert Neshkes and Dr. Stephen Read for allowing us to study their patients. Ms. Norene Hiekel and Ms. Vernie White prepared the manuscript. Dr. Houhhan is currently at the Psychology Service, VAMC Portland, Oregon. Address reprint requests to Jeffrey L. Cummings, M. D., West Los Angeles VAMC (Brentwood Division), Neurobehavior Unit, Ward 256b (69l/Bll l), 11301 Wilshire Boulevard, Los Angeles, CA 90073. 315 0093-934X/86 $3.OO Copyright 0 1986 by Academic Press, Inc. All rights of reproduction in any form reserved.
316
CUMMINGS,
HOULIHAN,
AND HILL
Dementia of the Alzheimer type (DAT) has been shown to produce a specific pattern of spoken verbal output resembling transcortical sensory aphasia and characterized by fluent verbalization, impaired comprehension, anomia, and preserved repetition (Schwartz, Marin, & Saffron, 1979; Appell, Kurtesz, & Fisman, 1982; Cummings, Benson, Hill, & Read, 1985). The reading abilities of DAT patients have been studied less exhaustively, but preliminary investigations have revealed that a dissociation of reading aloud and reading comprehension is common, with relative preservation of the ability to read aloud even when reading comprehension is severely compromised (Schwartz et al., 1979; Benson, Cummings, & Tsai, 1982; Cummings & Benson, 1983; Obler & Albert, 1984; Cummings et al., 1985). In a detailed case study, Schwartz and colleagues (1979) reported that their patient could apply grapheme-to-phoneme correspondence rules for nonwords and non-English words and correctly read English words with irregular spellings. Sevush (1984) described similar findings in a larger group of patients. Such abilities have not been explored in other DAT patients or related to the severity of intellectual decline in DAT. Further characterization of the reading abilities of DAT patients is of interest for several reasons. First, detailed analysis of reading in DAT may’ establish features that aid in distinguishing DAT from other dementing illnesses and that help identify the stage of advancement of the DAT. Second, the pattern of reading deterioration may help determine if reading comprehension deficits are based on perceptual deficits produced by disturbances at the visual-analytic level or are semantic comprehension deficits secondary to linguistic deterioration. Third, the reading characteristics may aid in deciding between two prevalent models of DAT: (1) dementia is a product of instrumental failures similar to the infarctioninduced aphasias, or (2) cognitive decline is a dedevelopmental process with a progressive de-differentiation of language skills. To help clarify these questions, a series of reading tasks was chosen and administered to DAT patients. SUBJECTS
The subjects consisted of 13 patients with DAT. They were 61 to 82 years old and all but one were right-handed. All had at least an eighthgrade education (range 8-16 years), and none of the reading tests (except the New Adult Reading Test as explained below) required reading skills beyond the elementary school level. All patients had vision adequate to allow unimpaired perception of the written stimuli. All subjects met Diagnostic and Statistical Manual of Mental Disorders (1980) criteria for primary degenerative dementia and National Institute of Neurologic and Communicative Disorders and Stroke criteria for probable DAT (Mckhann et al., 1984). None of the patients suffered from an active
READING
DETERIORATION
IN DEMENTIA
317
systemic illness or had evidence of an affective disorder, and all had a Hachinski Ischemia Scale score of 4 or less, consistent with degenerative dementia (Hachinski et al., 1975). The severity of dementia was assessed with the Mini-Mental State Examination (MMSE) (Folstein, Folstein, & McHugh, 1975), and a score of 24/40 or less was required for entry into the study. MMSE scores ranged from 1 to 19 (mean 10.0). READING TESTS AND RESULTS
Table 1 presents a summary of the reading test results. The tests and the group and individual response characteristics are described below. Tests of Reading Aloud Letter reading. The most elementary visual stimuli presented were letters. Each patient was asked to read aloud 30 randomly chosen letters: 10 uncomplicated letters, 10 incomplete letters, and 10 letters partially obscured by multiple diagonal lines. This skill was remarkably resistant to disruption by the dementia. Patients with MMSE scores of 5 or more read from 27 to 30 of the letters. Dividing the ordered sample into median (half the values fell below and half above), first quartile (Q, ; 25% below, 75% above), and third quartile (Q3-; 75% below, 25% above), the scores ranged only from 29 (Q3-) to 27.5 (Q,), and 11 of 13 patients scored above Q,. Two severely immpaired patients with MMSE scores of 4 and 1 correctly identified 20 and 24 of 30, respectively. Incomplete and obscured letters were read as easily as the uncomplicated presentation. Word reading. Each patient was asked to read aloud 30 high-frequency four-letter words and 10 prepositions. The 20 words consisted of 10 “emotional” words (e.g., kill, pain, rape), 10 concrete words (e.g., boat, suit, plug), and 10 abstract words (e.g., time, form, unit) matched for word frequency (Landis, Graves, Benson, & Hebben, 1983).Word reading ability was preserved in all but the most impaired patients. Eleven of the patients were able to read 38/40 words. The sample ranged from 38 (Q,) to 40 (Q-0 and only 2 of 13 patients scored below Q,. Only 2 patients had scores deviating markedly from 40 and they had MMSE scores of 6 and 1, respectively. A severely impaired patient with an MMSE of 4 performed the task perfectly. Reading obscured words. This word reading test was designed to help separate perceptual from linguistic deficits. Ten partially obscured words (words with several diagonal lines drawn through them) were presented. Such stimuli exaggerate the visual-perceptual deficits of patients with visual agnosia (Landis et al., 1982) but have little effect on the reading of DAT patients. Ten of the 13 patients read 9-lO/lO words, 3 patients with MMSE scores of 7, 6, and 1 read 4, 7, and O/10, respectively. The quartiles of the sample ranged from 8 (Q1) to 10 (QX), and 11 of 13 patients scored above Q,.
6
5
5
10
6
6
67
9
10
67
29 40
30 30
16
19
2
74
1
73
4
5
5
1
2
62
6
10
29 40
13
82
44
6
10
27 40
15
78
3
8
5
74
6
10
29 40
13
5 78
TEST INFORMATION
Note. Q,, quartile 1; M, median; Q,, quartile 3.
Reading comprehension Word vs. nonword recognition Following written commands Sentence comprehension
Reading aloud Letter reading Word Reading Reading obscured words Commands
Age: MMSE:
Patient information and tests
READING
TABLE I
6
4
78
6
10
29 38
12
6 74
4
6
65
6
10
29 40
10
7 JO
Patient
3
4
53
6
10
28 40
8
8 78
0
2
55
2
4
28 38
7
61
9
0
1
45
6
29 25 7
10 74 6
FROM 13 PATIENTS WITH DEMENTIA
5
2
62
6
10
28 39
76 5
11
3
0
52
6
20 40 9
78 4
12
0
0
47
0
24 0 0
1
77
13
OF THE ALZHEIMER
1
1
50
6
27.5 38 8
5.5
QI
TYPE
4
4
62
6
10
29 40
10
M
5.5
5
67
6
10
29 40
14
Q,
10
6
80
6
10
30 40
30
Best possible score
READING
DETERIORATION
IN DEMENTIA
319
Commands. Written commands from the Western Aphasia Battery (WAB) (Kertesz, 1979) were administered to all patients. Reading the commands aloud was performed perfectly by all except two of the subjects and these had MMSE scores of 7 and 1. Reading Comprehension Word vs. nonword recognition. In this test, each patient was shown 80 four-letter combinations. Using the method described by Patterson (1979), half the stimuli were English words and half were nonsense letter arrangements. The patient read the words aloud and indicated the nonword nature of the nonsense letter combinations. On this task, word discrimination skills were present to a limited extent even in the most deteriorated patient, but the discrimination ability declined as the dementia worsened in severity (correlation with MMSE: r = 5.02, p < .05). Understanding written commands. Comprehension of commands from the WAB was impaired, and there was a significant correlation with increasing severity of intellectual impairment (correlation with MMSE, r = .701, p < .005). Nine of the 13 patients could read aloud more commands than they could read with comprehension; in no case was the reverse pattern found. There was a significant difference between the ability of the patients to read commands aloud and their ability to comprehend what they read (t = 3.438, p < .005). Understanding sentences. Sentence comprehension was tested using sentences from the Boston Diagnostic Aphasia Examination (Goodglass & Kaplan, 1983). A perfect score of lO/lO was obtained by the least impaired DAT patient, but sentence comprehension declined steadily with advancing dementia (correlation with MMSE scores, r = .699, p < .005). New Adult Reading
Test
The New Adult Reading Test (NART) (Nelson & O’Connell, 1978) consists of 50 irregular words (e.g., psalm, heir, facade) that can be pronounced correctly only if the patient is familiar with them: they do not obey the usual grapheme-to-phoneme conversion rules. Performance on this task was more variable than on any other. Scores ranged from 39 to 0 with a mean of 17.2 (median 19.5). Inspection of the distribution of scores revealed no relation between test performance and dementia severity. When performing the test, patients either read the word correctly or failed to produce a response. Errors related to phonetic reading were not observed. DISCUSSION
The DAT patients in this study showed a consistent pattern of reading impairment. Reading letters and words aloud, reading partially obscured
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letters and words, reading irregular words and reading commands aloud, although failed by patients in the most advanced stages of dementia, were relatively preserved through most of the range of intellectual impairment and showed little association with declining MMSE scores. Reading comprehension, however, demonstrated no such selective sparing and all tests involving understanding of written material (distinguishing words from nonsense letter arrangements, performance of written commands, and sentence comprehension) all declined systematically with advancing dementia and correlated significantly with decreasing MMSE scores. The observations made in this study confirm and extend those made by previous investigators. In a case report, Schwartz et al. (1979) showed that their DAT patient could read nonwords and non-English words using appropriate English phonological rules; she could also read irregular English words correctly. Reading comprehension was not extensively studied, but the patient was partially successful in written word-picture matching. Studies of groups of carefully diagnosed DAT patients by Appell et al. (1982) and Cummings et al. (1985) found a dissociation between the ability to read aloud and reading comprehension. Reading both words and sentences aloud was preserved, whereas comprehension of written words, commands, and sentenceswas characteristically impaired. Sevush (1984) found a similar dissociation and concluded that the predominant reading defect in DAT was one of semantic processing. Thus, studies addressing this issue have consistently demonstrated that DAT patients are able to phonologically encode written verbal stimuli but have difficulty semantically decoding such material. Nelson and O’Connell (1978) capitalized on the preserved ability of dementia patients to read irregular words in constructing the NART. They found that this capacity was not significantly affected by the severity of intellectual impairment, and the patients’ ability to read aloud could thus be used to assess the size of their premorbid vocabulary and to estimate their premorbid intellectual level. The research subjects, however, were not limited to DAT and consisted of all subjects with atrophy on computerized tomograms of the head. In the study reported here, a more homogeneous group of clinically diagnosed DAT patients also showed relative preservation of reading irregular words of the NART, and the results support a lack of correlation between dementia severity and this reading ability. Demonstration of the consistency with which a distinction between reading aloud and reading comprehension occurs in DAT suggests that this pattern may be diagnostically useful. Clinical diagnosis of DAT has previously been subject to error rates of at least 18 to 30% (Ron, Toone, Garralda, & Lishman, 1979; Sulkava, Haltia, Paetau, Wikstrom, & Palo, 1983), and attention to the pattern of alterations occurring in spoken language and reading of dementia patients may help distinguish DAT
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from other causes of acquired intellectual impairment (Cummings & Benson, 1983; Cummings et al., 1985). In angular gyrus syndrome, a condition that may closely resemble DAT, for example, Benson et al. (1982) showed that reading aloud and reading comprehension were comparably impaired, and this contrasting pattern aided in distinguishing the syndrome from DAT. The dissociation of reading skills noted in the patients reported here correlates with the distribution of pathologic changes present in DAT. DAT produces its major neuropathological, neurochemical, and metabolic changes on the posterior regions of the cerebral hemispheres in the area of the temporoparieto-occipital junction region (Brun & Gustafson, 1978; Davies, 1978; Benson et al., 1983; Cummings & Benson, 1983; Chase et al., 1984). Focal brain insults in this area are known to dissociate the ability to read aloud and the ability to read with comprehension in the syndrome of transcortical sensory aphasia (Albert, Goodglass, Helm, Rubens, & Alexander, 1981). Thus, the pattern of deterioration of reading skills observed in DAT is a product of the geography of hemispheric involvement and can be used clinically to aid in the identification of the distribution of pathologic alterations characteristic of DAT. The results of this study also help to clarify the question of whether the difficulties experienced by the DAT patient are perceptual or linguistic in nature. Rochford (1971) proposed that the naming deficits exhibited by DAT patients were largely attributable to an impairment of visual recognition, and agnosia is frequently reported as a prominent symptom in DAT. The ability to read aloud, however, is a perceptual task and is preserved in DAT. Moreover, partial obscuration of words, a procedure that increases the reading difficulties of patients with visual agnosia (Landis et al., 1982), did not significantly affect the ability of DAT patients to read aloud. Throughout most of the course of DAT, perceptual disturbances play little role in the patient’s reading comprehension deficits, and the comprehension disturbance appears to reflect a deficit at the semantic decoding level. Patients in more advanced stages of DAT than those studied here may develop perceptual deficits that contribute to the eventual loss of the ability to read aloud. The most severely involved patient in the series (MMSE = 1) exhibited impairment in both reading aloud and reading comprehension, and the former may reflect a late occurring visual processing disturbance. Finally, the observations in this study bear on the central question of the nature of the intellectual impairment in DAT. It has been proposed that the mental deterioration of DAT is a progressive de-development toward a prelinguistic state in which all adult knowledge has been forgotten (Cherkin & Flood, 1983). Others have suggested that the cognitive abnormalities in DAT are best viewed as instrumental deficits similar to those occurring with focal cerebral cortical insults (Cummings & Benson,
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1983; Cummings, in press), As noted above, the linguistic syndrome exhibited by patients with DAT resembles transcortical sensory aphasia and is similar to that manifested by patients with insults in the posterior aspect of the left hemisphere (Albert et al., 1981). The reading pattern is dissimilar to that exhibited by children learning to read. The lack of correlation between severity of dementia and reading of irregular words on the NART is particularly important in this regard. In the process of reading acquisition, children make grapheme-to-phoneme conversions that lead to mispronunciation of irregular words. The DAT patients did not make such errors and performed better on the test than a de-developmental model would predict. Thus, the results of this study are most consistent with the view that the reading disability and, presumably, the other intellectual abnormalities in DAT are instrumental deficits produced by dysfunction of cortical areas crucial to specific intellectual skills. REFERENCES Albert, M. L., Goodglass, H., Helm, N. A., Rubens, A. B., & Alexander, M. P. 1981. Cinical aspects of dysphasia. New York: Springer-Verlag. Appell, J., Kertesz, A., & Fisman, M. 1982. A study of language functioning in Alzheimer patients. Brain and Language, 17, 73-91. Benson, D. F., Cummings, J. L., & Tsai, S. Y. 1982. Angular gyrus syndrome simulating Alzheimer’s disease. Archives of Neurology, 39, 616-620. Benson, D. F., Kuhl, D. E., Hawkins, R. A., Phelps, M. E., Cummings, J. L., & Tsai, S.Y. 1983. The fluorodeoxyglucose “F scan in Alzheimer’s disease and multi-infarct dementia. Archives of Neurology, 40, 711-714. Brun, A., & Gustafson, L. 1978. Limbic lobe involvement in presenile dementia. Archiv fur Psychiatric
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Hachinski, V. C., Iliff, L. D., Zilka, E., Du Boulay, G. H., McAllister, V. L., Marshall, J., Russell, R. W. R., & Symon, L. 1975. Cerebral blood flow in dementia. Archives of Neurology, 32, 632-637. Kertesz, A. 1979. Aphasia and associated disorders: Taxonomy, localization, and recovery. New York: Grune & Stratton. Landis, T., Graves, R., Benson, D. F., & Hebben, N. 1982. Visual recognition through kinaesthetic mediation. Psychological Medicine, 12, 515-531. Landis, T., Regard, M., Graves, R., & Goodglass, H. 1983. Semantic paralexia: A release 21, of right hemispheric function from left hemispheric control? Neuropsychologia, 359-364. McKhann, G., Drachman, D., Folstein, M., Katzman. R., Price, D., & Stadlan, E. M. 1984. Clinical diagnosis of Alzheimer’s disease: Reprt of the NINCDS-ADRDA work group under the auspices of the Department of Health and Human Service task force on Alzheimer’s disease. Neurology, 34, 939-944. Nelson, H. E., & O’Connell, A. 1978. Dementia: The estimation of premorbid intelligence using the New Adult Reading Test. Cortex, 14, 234-244. Obler, L. K, & Albert, M. C. 1984. Language is aging. In M. L. Albert (Ed.), Clinical neurology of aging. New York: Oxford Univ. Press. Pp. 245-253. Patterson, K. E. 1979. What is right with “deep” dyslexic patients? Brain and Language, 8, 111-129. Rochford, G. 1971. A study of naming errors in dysphasic and demented patients. Neuropsychologia,
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