P. Howlin*, L. Wing¹, J. Gould² *Correspondence to first author. ¹Department of Psychology, St George's Hospital Medical School, Tooting, London SW17 0RE, UK. ²Centre for Social and communication Disorders, Bromley, Kent, UK. Developmental Medicine and Child Neurology, 1995, 37, 406-414 |
Accepted for publication 19th July 1994. Reprinted with permission of the author. |
Although autism is a relatively rare occurrence in people with Down syndrome, there are an increasing number of reports of the two conditions co-existing. Wing and Gould (1979) carried out an epidemiological study of 35,000 children under the age of 15 years, using the Medical Research Council's Handicaps, Behaviour and Skills (HBS) interview schedule (Wing and Gould 1978). They initially reported one child from a total of 30 fully ambulant children who met two essential criteria for typical autism (Kanner and Eisenberg 1956) and another two children who were severely socially impaired, mute, with no pretend play and marked motor stereotypies. Although these two were within the autistic spectrum, they were not classified as having Kanner's autism because they showed no adherence to elaborate non-functional routines other than their motor stereotypies. At follow-up, it was clear that one more child with Down syndrome should have been included in the socially impaired but not typically autistic group (Kanner, personal communication). Turk (1992), also using the HBS schedule, reported that 9 per cent of his series of children with Down syndrome met the full ICD-10 criteria for autism (World Health Organization 1993). Ghaziuddin (personal communication) found autism in 10 per cent of his subjects with Downs' syndrome. Gillberg (1986) identified or child with 'classic' autism from a group of 20 children with Down syndrome Ghaziuddin et al. (1992) found two children who fulfilled DSM III-R criteria fit autism (American Psychiatric Association 1987) from an estimated total of 40 with Down syndrome (based on school-age population figures). Lund (1988), in a Danish epidemiologies study of 44 adults with Down syndrome diagnosed four males and one female a, having autism, again using the HBS questionnaire (Wing and Gould 1978).
A number of individual case studies are also reported in the literature. Ghaziuddin et al. (1992) described three cases with Down syndrome who met DSM-III-R criteria for autism and who scored well above the cut-off scores for autism on the Autism Behaviour Checklist (Krug at al. 1980). Two had severe mental impairment and the third was considered to have moderate intellectual impairment. All three had some language, although this was repetitive or non-communicative. Impairments in non-verbal skills, imaginative play, peer relationships and social interactions generally were also noted. Despite the generally low intellectual abilities of the subjects described, the stereotyped and repetitive behaviours they exhibited were not simply those typically associated with severe disability (which consist of principally motor mannerisms, stereotypies and self stimulatory behaviours); there was also evidence of the more complex rituals and routines characteristic of autism. These included insistence on repeating the same activities (playing the same records over and over, watching the same television programmes, and lining up and dusting objects), a strong resistance to environmental change, marked attachments to objects, and a tendency to touch or smell people and objects. Bregman and Volkmar (1988) described a 12-year-old girl with Down syndrome and non-verbal abilities in the severely retarded range. She met DSM-III and DSM-III-R criteria for autism and scored within the autistic range on the Childhood Autism Rating Scale (Schopler et al. 1986). Although she did not speak, she had a number of signs and gestures but failed to use these communicatively. Social interactions were markedly impaired and she exhibited many repetitive behaviours and preoccupation with the parts and details of objects. She also tended to smell toys and other objects and to feel them in her mouth.
The seven-year-old Japanese boy described by Wakabayashi (1979) was much more profoundly retarded, and diagnosis in this case is perhaps somewhat less clear-cut (he had, for instance, shown evidence of physical and motor regression at the age of two and a half years, and was now completely dependent on adults for all his needs). However, the author concluded that the boy met both Kanner's (1943) and Rutter (1965) criteria for autism.
The following case studies describe four boys aged between eight and eleven years, who were seen in early 1993. All had Down syndrome, but in each case the Parents had become concerned at their Children's failure to make progress and by the realization that, as they grew older, they clearly differed from their special peer group in many ways, especially in terms of their play and social and communication skills.
Child A, now aged l1 years 5 months, had been adopted at the age of 4 years 9 months by a single mother who had also successfully adopted another child with Down syndrome. Children B and C aged 9 years 11 months and 11 years 8 months, respectively, were being brought up by single divorced parents. Child D, aged eight years, lived with both parents. All children had been born in the UK.
Down syndrome was diagnosed at birth in all four cases, but whereas the children's additional physical problems were recognized and treated as necessary in the early years, the social, communication and behavioural abnormalities described by the parents seem to have received little attention.
All the children's parents had requested further assessment because they believed these additional problems could not simply be explained by the fact that the child had Down syndrome.
All the children had been placed initially in schools for pupils with severe learning disabilities. Child A bad been removed by his mother because she felt the structure was not appropriate to his needs and he had recently been accepted by a school for children with a mixture of communication and behavioural problems. The parents of B and C were also unhappy with the educational provision available, mainly because of the schools' failure to deal adequately with the children's social and communication problems and their ritualistic behaviour. For similar reasons the parents of child D were exploring the possibility of a transfer to a unit specializing in autism.
A detailed history of each child's early development was completed in collaboration with the parents. The first three cases were assessed using the HBS (Wing and Gould 1978); the fourth child was assessed using the Autism Diagnostic Interview (ADD) (Le Couteur el al. 1989). The children were also observed individually and formal psychometric assessments were attempted. All clearly fulfilled the diagnostic criteria for autism in terms of their social, play and communication difficulties and the presence of rituals and routines. Case D, for example, scored well above the cut-off levels for autism in all areas assessed on the ADD; thus his score for communication deficits was 13 (cut-off 8), for social impairments 28 (cut-off 11), and for repetitive and stereotyped behaviours 6 (cut-off 3). In all cases abnormalities in development had been noted in the first two to three years of life.
Because of their chromosomal abnormalities, the difficulties shown by the children had generally been attributed in the past to Down syndrome or their cognitive delays. However, it was evident that they differed in many ways from most other children with this condition. Their social relationships were much less well developed, attachments to adults were delayed; there was little evidence of shared attention, empathy or understanding of others' feelings, and they failed to use adults for comfort in the usual way. Relationships with other children were particularly poor and often characterized by aggression or resistance. Although three of the children had some speech, their language was abnormal, being echolalic or repetitive, and rarely used communicatively. For all children their main mode of communication was to take adults by the hand to indicate their needs.
Non-verbal skills such as eye contact and gesture were uniformly poor, and none of the four showed any spontaneous imaginative play. All the children showed stereotyped motor behaviours, which is common in children with severe learning disabilities. However, they also showed a striking resistance to change and an insistence on routines. Child A spent much of his time sorting objects into boxes and had very fixed routines, being happiest when sitting by a radiator, and listening to music tapes. He always listened to music before going to sleep, and the last piece heard in the evening had to be the first tune played the next day. Child B was so resistant to change of any kind that his playroom was empty of everything, including floor covering, except for his cassette recorder. If the school bus took a different route he would refuse to get off when it reached his home. Child C always insisted on sitting in specific places, and became very distressed on seeing anyone he knew in an unfamiliar setting; he was very upset when his mother bought a new car or changed the wallpaper, and his life was said to be 'dominated by his repetitive routines and resistance to change'. Child D was obsessed with toilets, light-switches, taps and doors, and although he was not toilet trained, the first thing he would do on entering anyone's house was find and then flush the lavatory. The only videos he watched were old 'Sooty and Sweep' shows, and he carried a Sweep puppet around with him at all times. Cups and chairs had to be placed in fixed position and he would only drink clear liquids such as mineral water or lemonade. In the garden he had a particular piece of hose pipe that he waved constantly back and forth (and which he always seemed able to find even if his parents hid it). For details of other routines, obsessions and attachments, etc., see Table III.
Child A | Child B | Child C | Child D | |
A. Social interaction-impaired in: | ||||
1. Awareness of others' feelings | + | + | + | + |
2. Seeking of comfort | + | + | + | + |
3. Imitation | + | + | + | + |
4. Social play | + | + | + | + |
5. Peer friendships | + | + | + | + |
B. Communication-impaired in: | ||||
1. Verbal or non-verbal communication | ||||
2. Use of non-verbal communication skills (eye-contact, etc.) | + | + | + | + |
3. Imagination | + | + | + | + |
4. Volume, pitch, intonation etc. of speech | NA | NA | NA | NA |
5. Content of speech: stereotyped, idiosyncratic, etc. | + | + | NA | + |
6. Conversational interchange | NA | NA | NA | NA |
C. Stereotyped routines | ||||
1. Motor stereotypies | + | + | + | + |
2. Preoccupation with parts of objects | + | + | + | + |
3. Distress over trivial changes | + | + | + | + |
4. Insistence on routines | + | + | + | + |
5. Preoccupation with one narrow interest | + | + | + | + |
Child A | Child B | Child C | Child D | |
A. Abnormal before 3 years of age in: | ||||
1. Social communication | + | + | + | + |
2. Social attachment and/or interaction | + | + | + | + |
3. Functional and/or symbolic play | + | + | + | + |
B1. Social interaction-impaired in: | ||||
a. Non-verbal social regulation | + | + | + | + |
b. Peer relationships | + | + | + | + |
c. Response to others' emotions; behaviour in social context: integration of social emotional and communicative behaviour | + | + | + | + |
d. Sharing pleasure with others | + | + | + | + |
B2. Communication-impaired in: | ||||
a. Verbal and non-verbal language | + | + | + | + |
b. Reciprocal conversation | NA | NA | NA | NA |
c. Meaningful language (i.e. language is stereotyped and repetitive) | + | + | NA | + |
d. Pretend play | + | + | + | + |
B3. Stereotyped routines: | ||||
a. Restricted patterns of interest | + | + | + | + |
b. Adherence to non-functional routines | + | + | + | + |
c. Motor stereotypies-hand/finger or whole body | + | + | + | + |
d. Preoccupation with part objects or quantities-feel, smell etc. | + | + | + | + |
Child A (11:5) | Child B (9:11) | Child C (11:8) | Child D (8:0) | |
Original Diagnosis | Down syndrome: infantile spasms | Down syndrome left hemi-hypertropy (affecting mainly the leg) | Down syndrome | Down syndrome |
Early development | Miserable; feeding problems. | Quiet, unresponsive except to lights | Quiet, unresponsive | Unresponsive |
Physical problems | Walked just before 5 yrs. Still has problems walking; nystagmus | Walked at 2 yrs; still has problems walking; odd gait; short-sighted; ambidextrous | Walked at 3 yrs; now runs on toes; heart condition(Fallot's tetralogy) | Walked at 30 mths; possible hearing loss; marked squint. |
Self-care | Poor; very dependent toilet-trained at 5 yrs. | Limited; not yet dry at night; does not chew food | Toilet-trained at 10; needs help with washing and dressing | Not toilet-trained; needs help with dressing, etc. |
Communication | Echoes; takes adults by hand though has Makaton signs and some words | Pulls people by hands; some echolalia; repeats words over and over | No words or consistent signs; pulls adults by hand | Repetitive, non- communicative; use of a few words; takes adults' hands; has signs but does not use |
Imagination | No spontaneous pretend play | No pretend play | No pretend play | No pretend play |
Social Development | Poor eye-contact; ignores or hits children; little show of affection. Does not come for comfort; dislikes physical contact | Poor eye contact; Aggressive to peers; hugs adults without discrimination; separation anxiety; very disinhibited; no shared attention | Poor eye contact, pushes other children; dislikes cuddles; shows no greeting behavior; little affection | Poor eye contact; no greeting or seeking comfort; pushes away other children; no shared attention |
Stereotypies | Jumps, rocks, and flaps; hand mannerisms | Flaps and rocks; makes odd noises | Jumps, flaps, spins and rocks | Flaps arms and waves head simultaneously |
Special interests | Audio-tapes; fitting things in boxes; specific videos | Thomas the Tank engine and Michael Jackson videos | Videos; spinning things; flickering candles | Toilets, taps, switches and doors. Watches Sooty and Sweep videos constantly |
Attachment to objects | Always something in hand | Leaves and sticks | Pink hair brush; other 'twiddlers' | 'Sweep' puppet; piece of hose-pipe |
Routines | Very fixed daily pattern; dislikes new clothes/foods/videos; distressed by change | Distressed at change in routes/routines, etc; Play room totally empty except for tape recorder | Hates any change to surroundings/routine. Insists on sitting in fixed places; upset if others in "wrong" | Obsessional use of toilets, lights, etc. Has fixed places for self and objects; drinks only clear liquids |
Behavior | Aggression, mood swings; resistant to demands/changes | Aggressive, destructive, tempers; overactivity | Running away; no sense of danger; throwing objects | Destructive; negativistic; provocative |
Psychometry | No co-operation | Leiter: 4 yrs | No co-operation | No co-operation |
Special skills | Amazing memory | No particular skills | Good memory | None |
Having first had to come to terms with the fact that their children had Down syndrome, the parents then had to cope with the realization that their children's deve1opment was abnormal even relative to their special peer group. Although the parents had frequently expressed concerns about their children's development, they had tended to be assured that this was all that could be expected. The parents of child D, for instance, had raised the possibility some years earlier that he might be autistic but school records show that staff were 'very reluctant' even to consider this. The professionals in these cases seemed to pay little heed to the fact that, linguistically and socially, the children were falling further and further behind other children with Down syndrome of the same age. Moreover, even if particular problems were acknowledged, these were often misinterpreted. For example, although the educational psychologist involved with child B noted that 'it would not do him justice to consider him as just an ordinary Down lad', and remarked on his odd relationships with people and objects in his environment and his need for order and routines, his behaviours seem to have been interpreted by the school as 'naughty' or 'willful'. Child D's problems were very clearly described by his teachers, but were viewed simply as 'difficult behaviours' and explained away in terms of poor motivation and lack of co-operation. School reports indicated no concerns about his social development and gave no indication that he was in any way different from his peers. However, they also noted that his motivation to communicate was 'on his terms only'; that he had 'quite definite likes and dislikes and routine is obviously important to him'; and that his cooperation was poor and he had a tendency to 'opt out' of group activities. He was also observed to place 'objects' in very specific places' and was only recently 'becoming more tolerant to touch and physical contact'.
The failure to appreciate the nature of children's learning, behavioural and social difficulties had obvious implications for teaching. For the children described here, there seems to have been a failure to recognise their need for a highly structured environment, involving individualized step-by-step teaching programmes, and in most cases there has been little if any awareness of their lack of social understanding or their need for specialist help to develop communication skills School reports for child D suggested the need to 'present him with opportunities to enrich the quality of his play activities; to share these with other children and to communicate .as often as possible'. Yet no specific strategies for teaching were suggested; nor was his failure to use the limited amount of language he possessed in any communicative way considered significant. However, simply presenting a child with autism with the 'opportunities' to learn is known to be ineffective. Only highly structured teaching specifically geared to the child's particular pattern of skills and deficits is likely to have any significant impact on outcome (Rutter and Baftak 1973, Howlin and Rutter 1987). Psychometric testing proved impossible in three of the four cases reported here (even if the child's own teacher was present) largely because of their lack of co-operation and their stereotyped behaviours. The psychologists involved (P.H. and J.G.) had wide experience of assessing children with autism but were nevertheless unsuccessful in their attempts to carry out formal assessments. If the children's educational needs had been recognised and appropriately catered for at a much earlier stage, such problems might have been avoided.
The finding of the co-occurrence of autism or autistic spectrum disorders contrasts with the usual view of people with Down syndrome as being sociable and outgoing. There is no published epidemiological study of the prevalence of autistic spectrum disorders in a large population of children with Down syndrome, but the evidence currently available suggests that it is in the region of 10 per cent for autism. The Camberwell epidemiological study found a total of 13 per cent for the whole spectrum but only 3 per cent for typical autism using the criteria of Kanner and Eisenberg, which tend to give the lowest rates (Wing 1993). The rates from the studies quoted for autistic disorder or autistic spectrum disorders are larger than for the population as a whole, even taking the highest estimate of around one in 200. This includes the rate for autistic spectrum disorders in children with learning disabilities (Wing and Gould 1979) plus the estimate for Asperger syndrome in children mostly with IQ of 70 or above (Ehlers and Gillberg 1993). A more realistic comparison group for the children with Down syndrome comprises those who have moderate, severe or profound learning disabilities (IQ of below 50), among whom the rates for autistic spectrum disorders are much higher than for the general population. In the Camberwell study, among the fully mobile children with IQ's of below 50 who did not have Down syndrome there were 16 per cent with Kanner's autism and 57 per cent with other autistic spectrum disorders. Thus children with Down syndrome seem more likely to be autistic or to have other autistic spectrum disorders than would be expected by chance on the basis of total population studies, but are less likely to have these disorders than other children with moderate, severe or profound learning disabilities.
In the present state of knowledge of the causes of autistic conditions, it is possible only to speculate on the aetiological implications of the association of autism and Down syndrome. Given the difference in prevalence rates noted above, it appears at first glance that autistic spectrum disorders in children with Down syndrome cannot be explained away as one of the hazards of having an IQ of below 50. However, in the Camberwell study (Wing and Gould 1979) it was found that 5 per cent of the fully mobile children with profound learning disabilities (IQ of below 20) had Kanner's autism and 90 per cent had other autistic spectrum disorders. If all the children with Down syndrome and autistic spectrum disorders had IQs of below 20, this might explain the association, though not why they had such profound disabilities. In the Camberwell study, three of the children with Down syndrome and an autistic spectrum disorder had profound learning disabilities and one was just above this level, whereas all those with Down syndrome. who were sociable were in the severe, moderate or (in one case) mild learning disability ranges. In the present paper, three of the children were untestable and probably had profound learning disabilities, although one was in the moderately disabled range. The levels of ability of the subjects with Down syndrome in the other papers quoted were not given in sufficient detail to allow specific conclusions to be drawn.
Another possibility is that additional medical disorders may be linked with the autism and the very low levels of ability which are not found in most children with Down syndrome. In the Camberwell study, the one child with Down syndrome and Kanner's autism had had infantile spasms and continued to have fits. Of the three with autistic spectrum disorders, all had congenital heart lesions (giving rise to recurrent episodes of cyanosis in at least one child), and two had severe visual impairments (one with myopia, nystagmus and strabismus and the other with cataracts). Among the four cases reported here, two had had serious medical conditions: infantile spasms in one case and a major heart condition (Fallot's tetralogy) in the other; this was repaired but the child remained under constant medical supervision. The other two both had squints and one possibly had hearing loss (Table III).
Details of associated medical conditions are not available for the other studies quoted, so no definite conclusions can be drawn. However, the possibility that such medical conditions are linked with the autistic spectrum disorders requires careful investigation. The hypothesis would be that Down syndrome itself does not give rise to the brain pathology underlying autism but that the additional medical conditions do affect the relevant parts or functions of the brain.
A further suggestion (Ghaziuddin, personal communication) is that children with Down syndrome and autistic spectrum disorders may be members of families with a high incidence of the latter.
Investigations are needed to establish the nature of the association between the conditions. These ideally should include family and genetic studies and the same types of brain imaging and postmortem examinations of brain pathology, as have been carried out in autism (Bauman and Kemper 1994). Such investigations were not done for the children described in the present paper and no published data arc currently available.
The fact that the co-occurrence of autism and Down syndrome is rare seems, unfortunately, to have resulted in the mistaken belief that the two never go together. Indeed, the frequency with which the two conditions co-exist may well be greater than previous studies suggest. All the cases described by Ghazinddin et al. (1992) were seen within the course of a year and the four cases presented above were seen over a period of a few weeks. Nevertheless, even when autistic symptoms are evident in a child with Down syndrome, these tend to be attributed to the associated learning difficulties rather than being adequately assessed in their own right. The diagnosis of autism in other children is usually made well before they reach school age (although of course there are exceptions to this) but diagnosis in Down syndrome tends to be much later. In the present cases the diagnosis of autism was not made until the ages of eight, nine and 11 years; the Wakabayashi (1979) case was seven years old; that of Bregman and Volkmar (1988) 12 years old; in the Ghaziuddin at al. (1992) study, the ages at diagnosis were 17, 14 and 21 years; and in the Lund (1988) study all were adults.
Late diagnosis, or indeed the failure to diagnose at all, may clearly have detrimental and long-term effects on the lives of affected children and their families. The parents of child D, for example, described their increasing dejection as they saw their son 'falling further and further behind', despite help from a private language therapist and a clinical psychologist, and they became convinced that this 'failure' was their own fault. Having access to professional advice from those experienced in the field of autism can be crucial in developing the child's skills, in minimising the impact of routines, obsessions and rituals. and in avoiding the secondary problems that are liable to develop if the child's needs are not adequately understood (Wing 1980, Howlin and Rutter 1987). Being put in touch with a local parent support group is also of great benefit to many parents. Above all, appropriate education is essential and although this need not necessarily entail specialist autistic provision, the nature of the child's social and communication deficits need to be recognized, understood and adequately catered for.
Finally, for the majority of parents the correct diagnosis, rather than being viewed as an additional burden, comes as a relief, often exonerating them from a sense of guilt that it was they who were the cause of their child's difficulties. (Piper and Howlin 1992). Many parents of children with autism already face a battle obtaining a diagnosis Smith et al. 1994); it is unacceptable to make the struggle even harder for families who know their child has another life-long disability. Rather than relying on stereotyped and unfounded notions of the sorts of problems that children with Down syndrome may or may not suffer, there is a need for more research into the expected frequency of additional conditions such as autism. Research into the physical problems associated with Down syndrome has resulted in individuals with this condition living much longer and happier lives than was the case 30 years ago (Carr 1994). The recognition of other developmental disorders that may occur (albeit infrequently) with Down syndrome, and the provision of appropriate services, could have an equally beneficial impact on those with a dual disability.
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