Joumal of Intellectual Disability Research, 1992, 36, 241-250
Ageing in higher functioning adults with Down*s syndrome: an interim report in a longitudinal study D. A. DEVENNY, A. L. HILL, O. PATXOT, W. P. SILVERMAN AND K. E. WISNIEWSKI New York State Institute for Basic Research in Developmental Disabilities, Staten Island New York, USA ABSTRACT. Mildly and moderately mentally retarded adults, who live in the community, were examined for global changes in mental status and specific changes in auditory and visual memory over a period of 3-5 years. Twenty-eight subjects with Down's syndrome (DS) between the ages of 27 arid 55 years were compared to 18 subjects without DS who were of similar IQ and age. The evaluation of mental status consisted of testing orientation to person, place and time, object naming, visuomotor coordination, and concentration. Auditory memory was tested with an adapted version of the Buschke Memory test. Visual memory testing consisted of matching shapes which were presented simultaneously and after delays of 0, 5 and 10s on a computer-controlled screen. No changes were found in test scores between an initial testing and follow-up testing up to 5 years later, indicating that ageing processes were not having a major impact in the cognitive functioning of these subjects. Furthermore, there was no indication of any generalized decline in performance suggestive of early symptoms of dementia among the older subjects with DS.
INTRODUCTION Premature ageing has been recognized among people with Down's syndrome (DS) since a report by Fraser & Mitchell (1879). Until recently, however, ageing among this population was not considered to be an important issue affecting major programme development because people with DS typically were not expected to live past adolescence or young adulthood (Thase, 1982). Recent advances in medicine and changing attitudes towards the care of mentally retarded people have prolonged the life span of people with DS. Current life expectancy is 30 years for the 80% of people with DS without congenital heart defects (Baird & Sadovnick, 1987), and 25% of this population is now expected to survive past the age of 50 years (Thase, 1982). Therefore, understanding the course of development over the entire life span for people with DS, and describing any declines in functioning among these people that reflect a normal course of ageing, have now become important applied research goals. Numerous clinical signs which are associated with normal ageing, including postural changes, wrinkling of the forehead, deposition of ageing pigment and cataract formation have been described as occurring prematurely in adults with DS Correspondence: Dr Darlynne A. Devenny, NYS Institute for Basic Research, 1050 Forest Hill Road, Staten Island, NY 10314, USA. 241
242 D. A. Devenny et al. (see Oliver & Holland, 1986, for a recent review). Similarly, behavioural studies have demonstrated declines in cognitive and social functioning with onset not before 35 years of age (Fenner et al., 1987; Thase et al., 1984; Wisniewski et al., 1978; Zigman et al., 1987). However, the age at which declines in functioning in older people with DS can be demonstrated may be related to the specificity of the examinations used. Studies which have used behavioural scales have tended to show that the onset of decline in functioning in adults with DS, as compared to their peers, begins at a later age than those studies which have directly examined functioning. Specifically, Silverstein et al. (1988) found a relative decline in institutionalized adults with DS on a motor development factor after the age of 60 years, while Zigman et al. (1987) found adults with DS over 50 years of age were relatively poorer on both activities of daily living and cognitive skills. Fenner et al. (1987) used scores from the Stanford-Binet test and found a higher proportion of subjects over the age of 45 years declined relative to their highest past performance on this test than subjects below this age. On a battery of tests which included both general measures of attention, orientation and cooperation as well as specific measures of memory, Thase et al. (1984) concluded that adults with DS over the age of 50 years performed more poorly than subjects in the younger decades. Among their findings, however, was a reversal in the trend towards decline with age by what appears to be a higher functioning group in the age range of 41-50 years. There is the possibility that if the subjects in the 41-50-year-old group had been equated with the other age groups on some global measure of level of functioning, a decline in performance on specific psychological tests would have been identified at ages younger than 50 years. Using an extensive neuropsychological battery of tests, Haxby (1989) found that adults with DS 37 years of age and older performed at a lower level than younger subjects on tests requiring the formation of new long-term memories and visuospatial constructions. However, all of these studies have used cross-sectional research designs, thus introducing possible cohort and healthy survivor effects as confounds. Previous studies have selected subjects predominantly at the severe or profound level of mental retardation, but the wisdom of generalizing findings from these studies to all people with DS is questionable. To date, there is relatively sparse information on the course of normal ageing in mildly and moderately mentally retarded adults with DS. Indeed, it is not yet clear whether the physiological processes associated with premature ageing operate in similar ways in the extremes of functional levels. Zigman et al. (1987) partitioned their subjects by level of mental retardation and found on the cognitive skills factor of a behavioural scale that subjects in the mild/ moderate mentally retarded group were judged to show the same declines in abilities with increasing age as did subjects in the severe group, but fhis finding was not specific to people with DS. In the non-retarded population, declines in functioning due to normal ageing processes are distinguishable from the declines associated with dementing processes such as occur with Alzheimer disease (Bayles & Kaszniak, 1987). Because the neuropathology characteristic of Alzheimer disease has been found to occur precociously in people with DS (see Kemper, 1988, for a recent review), examination of the normal course of ageing in individuals with DS has been overshadowed by the
Ageing with Down's syndrome 243
quest for signs of early dementia. The prospective studies which have examined the onset and course of dementia of the Alzheimer type in people with DS have found that memory loss is an early indicator of subsequent deterioration in functioning. Dalton & Crapper McLachlan (1984), using a visual matching to sample test they developed for use with severely and profoundly retarded individuals, found that 25% of their subjects with DS who were over 40 years of age had memory impairment on their test. Lai & Williams (1989) reported that memory impairments could be detected as the first sign of dementia, but only in their subjects with mild and moderate mental retardation. Retrospective studies have typically shown incomplete concordance between neuropathology and clinicalfindings(see Thase, 1988, for a recent review). The suggestion has frequently been made that symptoms of early dementia, such as memory loss, are difficult to detect among people with mental retardation, and that application of more sensitive diagnostic measures will provide evidence for a closer association between neuropathology and early signs of Alzheimer disease (Haxby, 1989; Miniszek, 1983; Lai & Williams, 1989; Wisniewski et al., 1987). Therefore, the present authors undertook to examine adults with mental retardation to determine whether early signs of ageing and/or dementia could be detected by using a variety of psychological measures which should be sensitive to subtle changes in memory and overall cognitive functioning. In order to ensure that early symptoms would be detected, all prospective subjects were screened initially for any history of functional loss, and only people with no history of regression were included in the study. METHOD j
Subjects All subjects were participants in an ongoing study designed to evaluate changes in functioning associated with ageing among mentally retarded adults. They werei employed in sheltered workshops and lived in the community. Criteria for selection in the present study included age over 25 years, 10 greater than 35, no severe sensory impairments, and no suspicion of dementia by caretakers or workshop supervisors when the subject entered the study.' All subjects have been tested at least twice, with assessments spanning a range of no less than 3 years (mean=41 years). In this paper, initial test results of the subjects were compared with their most recent test results. An effort was made to include all workshop clients with DS who met the selection criteria at each facility visited. To ensure that no decline in functioning occurred prior to acceptance in the study, all available past 10 records of the subjects were compared to their most recent IQ test.
'Every effort was made to include all subjects who met the acceptance criteria at each facility we tested. Approximately 10% of potential subjects refused to participate or their families refused permission for testing. The basis for these refusals was personal and varied and not due to agerelated changes in functioning. One subject, a 60-year-old male with DS, was eliminated after the first testing when he developed bilateral cataracts which resulted in total loss of vision. Six subjects were lost to the study when they moved. An informal follow-up of these people indicated no changes in overall functioning.
244 D. A. Devenny et al. The present study included 28 adults with DS, and their performance on test tasks was compared to that of a second group of 18 subjects with mental retardation without DS. These two subject groups were divided into two subgroups based on their age at initial testing (age below or above 35 years). The characteristics of the four subject groups (etiology by age) are given in Table 1. Procedure Testing was conducted in a quiet, well-lit room at either the workshop or the residence of each client. Each session consisted of an interview to complete questions on mental status and two experimental tasks to test auditory and visual memory. A test session was approximately one hour in length. Subjects were paid $4 per hour of testing time. Tests The Evaluation of Mental Status consisted of 37 items. Subjects were asked 15 questions which tested orientation to person, place and time; four colours were named; 10 itenis tested naming on demand of parts and wholes of familiar objects. Each of these items was given a score of 2 for a spontaneous, correct answer and a score of 1 for choosing the correct answer from a choice of three items. In addition to these items, the subject was asked to recite the alphabet, to count to 30 forwards and to count from 20 backwards. Visuomotor control was measured by the printing of the letters A to E, the numbers 1 to 5 and drawing a circle, square and diamond. A spontaneous correct response was given a score of 2, and a correct copying from a model a score of 1 (Wisniewski & Hill, 1985). The Buschke Memory Test (Buschke, 1973) was modified for administration to mentally retarded adults (Hill et al. 1988) and this version was used to assess auditory memory. For this test, the subject was read a list of eight animal names (goat, cat, bear, cow, mouse, sheep, rabbit and monkey) and was then asked to repeat them using a typical free-recall procedure. Only those animal names which were omitted on the first naming trial were presented on a subsequent trial by the examiner and these were presented in the original order. The subject was then asked to repeat all the animals including those previously recalled. This basic procedure was repeated, with each subsequent trial presentation including animals which were omitted on the immediately preceding trial. This selective reminding procedure was repeated for 10 Table 1. Description of subjects at the time of initial testing Age (years)
IQ
Subject group
n
Mean
Range
Mean
Range
Down's syndrome: ^35 years >35 years Comparison: 35 years
12 16 5 13
31-7 41-8 31-0 44-1
27-34 36-55 27-35 36-58
54-5 55-8 58-4 56-3
41-77 45-64 43-68 35-81
Ageing with Down's syndrome 245 trials. The Buschke Memory Test provides multiple measures of memory processing capacity (Buschke, 1973). In the present study, two measures were selected to assess change between the two test times. The first measure was the number correct on trial one as a measure of immediate memory. The second measure was the total of items correct across the first nine trials, and represents a global measure of proficiency in encoding and retrieving information from memory. A Visual Memory Test was based on a task developed by Dalton et al. (1984) which was found to be sensitive to age associated changes in memory in older mentally retarded adults. The test used in the current study was intended to measure immediate recall for items not easily coded verbally, and consisted of a visual matching to sample procedure (Silverman et al., 1989). In the test, a target shape was presented on a videomonitor for 3 s. The task required matching the target shape to one of three shapes presented below the target shape. Subjects were required to point to their choice among the response stimuli. The stimulus shapes were all rectangles which varied in colour (blue or orange), shape (square of 15 cm, a rectangle of l"5x3'O cm or a rectangle of 1 •5x6-0 cm), orientation (horizontal or vertical) and configuration (the rectangle was filled or represented by an outline). The two foils were selected randomly. There were four conditions within the task, defined by the time elapsing between target offset and presentation of the response choices. The target could appear simultaneously with response choices and remain present until a response was made, or the target shape could be presented for 3 s, followed by the response choices after no delay, a 5-s delay or a 10-s delay. Presentation order of the four test conditions was counterbalanced using a Latin square design, and testing consisted of a total of 48 trials. Stimuli were presented on an Apple IIC computer connected to a 30-5 cm monitor at a distance of 46 cm from the subject. Training for the task consisted of repeated presentations of the simultaneous presentation condition until the subject could match the target shape with the correct response choice spontaneously.
RESULTS The first stage of analysis compared performance of the four groups (younger and older adults with and without DS) on each of the tests to examine changes between the initial and current testing. If any significant changes were found over the 3-5 year interest interval, further analyses were planned to determine in more detail how a specific change was related to age and/or the presence of DS. Mental status All subjects were able to answer most questions on the Evaluation of Mental Status, indicating satisfactory orientation to person, place and time, and ability to name objects. An analysis of variance (diagnostic group by age group by test session) indicated no differences for questions related to orientation to person, time, color or concentration. A significant effect of test session was found for questions relating to place [F(l, 42)= 13-313, P
Ageing in higher functioning adults with Down*s syndrome: an interim report in a longitudinal study D. A. DEVENNY, A. L. HILL, O. PATXOT, W. P. SILVERMAN AND K. E. WISNIEWSKI New York State Institute for Basic Research in Developmental Disabilities, Staten Island New York, USA ABSTRACT. Mildly and moderately mentally retarded adults, who live in the community, were examined for global changes in mental status and specific changes in auditory and visual memory over a period of 3-5 years. Twenty-eight subjects with Down's syndrome (DS) between the ages of 27 arid 55 years were compared to 18 subjects without DS who were of similar IQ and age. The evaluation of mental status consisted of testing orientation to person, place and time, object naming, visuomotor coordination, and concentration. Auditory memory was tested with an adapted version of the Buschke Memory test. Visual memory testing consisted of matching shapes which were presented simultaneously and after delays of 0, 5 and 10s on a computer-controlled screen. No changes were found in test scores between an initial testing and follow-up testing up to 5 years later, indicating that ageing processes were not having a major impact in the cognitive functioning of these subjects. Furthermore, there was no indication of any generalized decline in performance suggestive of early symptoms of dementia among the older subjects with DS.
INTRODUCTION Premature ageing has been recognized among people with Down's syndrome (DS) since a report by Fraser & Mitchell (1879). Until recently, however, ageing among this population was not considered to be an important issue affecting major programme development because people with DS typically were not expected to live past adolescence or young adulthood (Thase, 1982). Recent advances in medicine and changing attitudes towards the care of mentally retarded people have prolonged the life span of people with DS. Current life expectancy is 30 years for the 80% of people with DS without congenital heart defects (Baird & Sadovnick, 1987), and 25% of this population is now expected to survive past the age of 50 years (Thase, 1982). Therefore, understanding the course of development over the entire life span for people with DS, and describing any declines in functioning among these people that reflect a normal course of ageing, have now become important applied research goals. Numerous clinical signs which are associated with normal ageing, including postural changes, wrinkling of the forehead, deposition of ageing pigment and cataract formation have been described as occurring prematurely in adults with DS Correspondence: Dr Darlynne A. Devenny, NYS Institute for Basic Research, 1050 Forest Hill Road, Staten Island, NY 10314, USA. 241
242 D. A. Devenny et al. (see Oliver & Holland, 1986, for a recent review). Similarly, behavioural studies have demonstrated declines in cognitive and social functioning with onset not before 35 years of age (Fenner et al., 1987; Thase et al., 1984; Wisniewski et al., 1978; Zigman et al., 1987). However, the age at which declines in functioning in older people with DS can be demonstrated may be related to the specificity of the examinations used. Studies which have used behavioural scales have tended to show that the onset of decline in functioning in adults with DS, as compared to their peers, begins at a later age than those studies which have directly examined functioning. Specifically, Silverstein et al. (1988) found a relative decline in institutionalized adults with DS on a motor development factor after the age of 60 years, while Zigman et al. (1987) found adults with DS over 50 years of age were relatively poorer on both activities of daily living and cognitive skills. Fenner et al. (1987) used scores from the Stanford-Binet test and found a higher proportion of subjects over the age of 45 years declined relative to their highest past performance on this test than subjects below this age. On a battery of tests which included both general measures of attention, orientation and cooperation as well as specific measures of memory, Thase et al. (1984) concluded that adults with DS over the age of 50 years performed more poorly than subjects in the younger decades. Among their findings, however, was a reversal in the trend towards decline with age by what appears to be a higher functioning group in the age range of 41-50 years. There is the possibility that if the subjects in the 41-50-year-old group had been equated with the other age groups on some global measure of level of functioning, a decline in performance on specific psychological tests would have been identified at ages younger than 50 years. Using an extensive neuropsychological battery of tests, Haxby (1989) found that adults with DS 37 years of age and older performed at a lower level than younger subjects on tests requiring the formation of new long-term memories and visuospatial constructions. However, all of these studies have used cross-sectional research designs, thus introducing possible cohort and healthy survivor effects as confounds. Previous studies have selected subjects predominantly at the severe or profound level of mental retardation, but the wisdom of generalizing findings from these studies to all people with DS is questionable. To date, there is relatively sparse information on the course of normal ageing in mildly and moderately mentally retarded adults with DS. Indeed, it is not yet clear whether the physiological processes associated with premature ageing operate in similar ways in the extremes of functional levels. Zigman et al. (1987) partitioned their subjects by level of mental retardation and found on the cognitive skills factor of a behavioural scale that subjects in the mild/ moderate mentally retarded group were judged to show the same declines in abilities with increasing age as did subjects in the severe group, but fhis finding was not specific to people with DS. In the non-retarded population, declines in functioning due to normal ageing processes are distinguishable from the declines associated with dementing processes such as occur with Alzheimer disease (Bayles & Kaszniak, 1987). Because the neuropathology characteristic of Alzheimer disease has been found to occur precociously in people with DS (see Kemper, 1988, for a recent review), examination of the normal course of ageing in individuals with DS has been overshadowed by the
Ageing with Down's syndrome 243
quest for signs of early dementia. The prospective studies which have examined the onset and course of dementia of the Alzheimer type in people with DS have found that memory loss is an early indicator of subsequent deterioration in functioning. Dalton & Crapper McLachlan (1984), using a visual matching to sample test they developed for use with severely and profoundly retarded individuals, found that 25% of their subjects with DS who were over 40 years of age had memory impairment on their test. Lai & Williams (1989) reported that memory impairments could be detected as the first sign of dementia, but only in their subjects with mild and moderate mental retardation. Retrospective studies have typically shown incomplete concordance between neuropathology and clinicalfindings(see Thase, 1988, for a recent review). The suggestion has frequently been made that symptoms of early dementia, such as memory loss, are difficult to detect among people with mental retardation, and that application of more sensitive diagnostic measures will provide evidence for a closer association between neuropathology and early signs of Alzheimer disease (Haxby, 1989; Miniszek, 1983; Lai & Williams, 1989; Wisniewski et al., 1987). Therefore, the present authors undertook to examine adults with mental retardation to determine whether early signs of ageing and/or dementia could be detected by using a variety of psychological measures which should be sensitive to subtle changes in memory and overall cognitive functioning. In order to ensure that early symptoms would be detected, all prospective subjects were screened initially for any history of functional loss, and only people with no history of regression were included in the study. METHOD j
Subjects All subjects were participants in an ongoing study designed to evaluate changes in functioning associated with ageing among mentally retarded adults. They werei employed in sheltered workshops and lived in the community. Criteria for selection in the present study included age over 25 years, 10 greater than 35, no severe sensory impairments, and no suspicion of dementia by caretakers or workshop supervisors when the subject entered the study.' All subjects have been tested at least twice, with assessments spanning a range of no less than 3 years (mean=41 years). In this paper, initial test results of the subjects were compared with their most recent test results. An effort was made to include all workshop clients with DS who met the selection criteria at each facility visited. To ensure that no decline in functioning occurred prior to acceptance in the study, all available past 10 records of the subjects were compared to their most recent IQ test.
'Every effort was made to include all subjects who met the acceptance criteria at each facility we tested. Approximately 10% of potential subjects refused to participate or their families refused permission for testing. The basis for these refusals was personal and varied and not due to agerelated changes in functioning. One subject, a 60-year-old male with DS, was eliminated after the first testing when he developed bilateral cataracts which resulted in total loss of vision. Six subjects were lost to the study when they moved. An informal follow-up of these people indicated no changes in overall functioning.
244 D. A. Devenny et al. The present study included 28 adults with DS, and their performance on test tasks was compared to that of a second group of 18 subjects with mental retardation without DS. These two subject groups were divided into two subgroups based on their age at initial testing (age below or above 35 years). The characteristics of the four subject groups (etiology by age) are given in Table 1. Procedure Testing was conducted in a quiet, well-lit room at either the workshop or the residence of each client. Each session consisted of an interview to complete questions on mental status and two experimental tasks to test auditory and visual memory. A test session was approximately one hour in length. Subjects were paid $4 per hour of testing time. Tests The Evaluation of Mental Status consisted of 37 items. Subjects were asked 15 questions which tested orientation to person, place and time; four colours were named; 10 itenis tested naming on demand of parts and wholes of familiar objects. Each of these items was given a score of 2 for a spontaneous, correct answer and a score of 1 for choosing the correct answer from a choice of three items. In addition to these items, the subject was asked to recite the alphabet, to count to 30 forwards and to count from 20 backwards. Visuomotor control was measured by the printing of the letters A to E, the numbers 1 to 5 and drawing a circle, square and diamond. A spontaneous correct response was given a score of 2, and a correct copying from a model a score of 1 (Wisniewski & Hill, 1985). The Buschke Memory Test (Buschke, 1973) was modified for administration to mentally retarded adults (Hill et al. 1988) and this version was used to assess auditory memory. For this test, the subject was read a list of eight animal names (goat, cat, bear, cow, mouse, sheep, rabbit and monkey) and was then asked to repeat them using a typical free-recall procedure. Only those animal names which were omitted on the first naming trial were presented on a subsequent trial by the examiner and these were presented in the original order. The subject was then asked to repeat all the animals including those previously recalled. This basic procedure was repeated, with each subsequent trial presentation including animals which were omitted on the immediately preceding trial. This selective reminding procedure was repeated for 10 Table 1. Description of subjects at the time of initial testing Age (years)
IQ
Subject group
n
Mean
Range
Mean
Range
Down's syndrome: ^35 years >35 years Comparison: 35 years
12 16 5 13
31-7 41-8 31-0 44-1
27-34 36-55 27-35 36-58
54-5 55-8 58-4 56-3
41-77 45-64 43-68 35-81
Ageing with Down's syndrome 245 trials. The Buschke Memory Test provides multiple measures of memory processing capacity (Buschke, 1973). In the present study, two measures were selected to assess change between the two test times. The first measure was the number correct on trial one as a measure of immediate memory. The second measure was the total of items correct across the first nine trials, and represents a global measure of proficiency in encoding and retrieving information from memory. A Visual Memory Test was based on a task developed by Dalton et al. (1984) which was found to be sensitive to age associated changes in memory in older mentally retarded adults. The test used in the current study was intended to measure immediate recall for items not easily coded verbally, and consisted of a visual matching to sample procedure (Silverman et al., 1989). In the test, a target shape was presented on a videomonitor for 3 s. The task required matching the target shape to one of three shapes presented below the target shape. Subjects were required to point to their choice among the response stimuli. The stimulus shapes were all rectangles which varied in colour (blue or orange), shape (square of 15 cm, a rectangle of l"5x3'O cm or a rectangle of 1 •5x6-0 cm), orientation (horizontal or vertical) and configuration (the rectangle was filled or represented by an outline). The two foils were selected randomly. There were four conditions within the task, defined by the time elapsing between target offset and presentation of the response choices. The target could appear simultaneously with response choices and remain present until a response was made, or the target shape could be presented for 3 s, followed by the response choices after no delay, a 5-s delay or a 10-s delay. Presentation order of the four test conditions was counterbalanced using a Latin square design, and testing consisted of a total of 48 trials. Stimuli were presented on an Apple IIC computer connected to a 30-5 cm monitor at a distance of 46 cm from the subject. Training for the task consisted of repeated presentations of the simultaneous presentation condition until the subject could match the target shape with the correct response choice spontaneously.
RESULTS The first stage of analysis compared performance of the four groups (younger and older adults with and without DS) on each of the tests to examine changes between the initial and current testing. If any significant changes were found over the 3-5 year interest interval, further analyses were planned to determine in more detail how a specific change was related to age and/or the presence of DS. Mental status All subjects were able to answer most questions on the Evaluation of Mental Status, indicating satisfactory orientation to person, place and time, and ability to name objects. An analysis of variance (diagnostic group by age group by test session) indicated no differences for questions related to orientation to person, time, color or concentration. A significant effect of test session was found for questions relating to place [F(l, 42)= 13-313, P
