Developmental dissociation, deviance, and delay: occurrence of attentiondeficit hyperactivity
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1 Developmental dissociation, deviance, and delay: occurrence of attentiondeficit hyperactivity disorder in individuals with and without borderline-to-mild intellectual disability Robert G Voigt* MD; William J Barbaresi MD, Division of Developmental and Behavioral Pediatrics, Department of Pediatric and Adolescent Medicine; Robert C Colligan PhD, Department of Psychology and Psychiatry; Amy L Weaver MS; Slavica K Katusic MD, Department of Health Sciences Research, Mayo Clinic, Rochester, MN, USA. *Correspondence to first author at Division of Developmental and Behavioral Pediatrics, Department of Pediatric and Adolescent Medicine, Mayo Clinic, Baldwin 3A, 200 First Street SW, Rochester, MN 55905, USA. voigt.robert@mayo.edu A neurodevelopmental model for understanding the spectrum of developmental disabilities postulates that developmental delay, dissociation, and deviance reflect underlying central nervous system dysfunction. In this study, we determined the occurrence of the dissociated and developmentally deviant behavioral profile of attention-deficit hyperactivity disorder () among children with and without developmental cognitive delays (borderline-to-mild intellectual disability) in a population-based birth cohort (n=5718). Among the 70 children identified to have borderline-to-mild intellectual disability, 30% (n=21; 7 females, 14 males) met research criteria for, compared to only 6.4% of children without intellectual disability (n=358; 88 females, 270 males). The odds ratio for comorbid for children with versus without borderline-to-mild intellectual disability was 6.3 (95% confidence interval: ; p<0.001). These data illustrate that developmental dissociation and/or deviance, as represented by, are more likely to occur in the context of developmental delay, represented by borderline-to-mild intellectual disability. Developmental disabilities occur along a spectrum from high-incidence, low-morbidity neurobehavioral disorders, such as attention-deficit hyperactivity disorder (), to low-incidence, high-morbidity intellectual disabilities, such as mental retardation.* Capute and Accardo 1 have described a neurodevelopmental model for understanding the spectrum of developmental disabilities by means of an analysis of three fundamental neurodevelopmental processes: delay, dissociation, and deviance. Developmental delay refers to a significant lag in the attainment of developmental milestones, with global intellectual and adaptive delays representing the primary neurodevelopmental process underlying mental retardation. Developmental dissociation describes a significant difference between the developmental rates of two streams of development, with one stream significantly more delayed. Using Capute s triangle of three primary developmental streams (motor, cognitive, and neurobehavior), can be conceptualized as representing a dissociation between a child s overall level of cognitive ability and his or her behavior in the domains of attention, impulse control, or activity. 1,2 Developmental deviance occurs with behavior that is atypical at any age or is non-sequential over time. 3 can also then be conceptualized as representing an example of developmental deviance, because the impairing levels of inattention and impulsivity and the non-goal-directed hyperactivity exhibited by children with might be considered atypical at any age. 2,3 This neurodevelopmental model postulates that developmental delay, dissociation, and deviance reflect underlying dysfunction in the central nervous system. Consequently, dissociation and deviance should occur more commonly in association with more significant delays., conceptualized in this model by both dissociation and deviance, should, therefore, be more commonly recognized in children with intellectual disability than in those without such disability. However, evidence to support this model is lacking, because the epidemiology of in individuals with intellectual disability has not been well studied. 4 In this study we, therefore, tested the hypothesis that developmental dissociation and/or deviance () occur more commonly in children with developmental delay (intellectual disability) in a population-based birth cohort. Method STUDY SETTING AND PARTICIPANTS The capacity for a population-based study of the occurrence of in children with and without borderline-to-mild intellectual disability is the result of a unique set of circumstances and resources available in Rochester, MN. Through a contractual research agreement, permission was obtained to access the cumulative school records for every child born in Rochester between 1 January 1976 and 31 December 1982 to mothers residing in Independent District no. 535 (Rochester, MN). Through the Rochester Epidemiology Project, we also had access to the complete medical records for all members of this birth cohort. 5 Medical records are available from the Mayo Clinic, the Olmsted Medical Center, and the few private medical practitioners in the community, encompassing essentially all of the providers of primary and specialty medical care for residents of Rochester. The medical *UK usage: learning disability. Developmental Medicine & Child Neurology 2006, 48:
2 records contain the detailed history of all medical encounters in the community, including ambulatory, medical, and social services, hospitalizations, emergency department, and home visits, as well as laboratory, psychiatry, and psychology reports and test results, from birth until the patient no longer resided in the community. Descriptions of the processes for identification of the 5718 members of the birth cohort who remained in Rochester at least until the age of school entry, and who were included as participants for this study, have been published previously. 6,7 Patient authorization for use of medical records for research purposes was obtained in accordance with Minnesota statutes, and approved by the Mayo Institutional Review Board. IDENTIFICATION OF INCIDENT CASES USING RESEARCH CRITERIA Detailed descriptions of the methods used to identify incident cases of and intellectual disability in this birth cohort have already been published. 6 8 A summary of the methods used to identify cases follows (Fig. 1). A five-step approach was employed, beginning with a review of school records for evidence of any concern about learning or behavior. records for all 5718 children were reviewed, regardless of whether the child had any specific clinical diagnosis, including. This yielded 1951 children with recorded learning or behavioral concerns. In the second step we ed additional information from school and medical records, including symptoms of as specified in the Diagnostic and Statistical Manual of Mental Disorders 4th Edition (DSM-IV), 9 results from teacher and/or parent questionnaires, and clinical diagnoses of. A total of 1171 children had at least one of these four types of information documented in their school and/or medical records. In the third step, for the 3767 children whose school records did not include any suggestion of learning or behavioral problems, we searched the computerized index of medical diagnoses, which captures diagnoses on all patients seen at the Mayo Clinic and the Olmsted Medical Center, for diagnoses related to and including. This identified 169 additional children as potential incident cases. In the fourth step we reviewed II step / medical record I step record review 1171 In study 5718 performance concern yes performance concern no 3767 III step Medical record 169 Medical diagnostic index 3598 IV step Medical record 4 Private psychiatry group 3763 Figure 1: Flow diagram describing steps in identification of children with attentiondeficit hyperactivity disorder () in the 1976 to 1982 birth cohort, Rochester, MN. Reprinted from Annals of Epidemiology, 15(6): Katusic SK, Barbaresi WJ, Colligan RC, Weaver AL, Leibson CL, Jacobsen SJ. (2005) Case definition in epidemiologic studies of AD/HD. Copyright (2005), with permission from Elsevier. V step Identification of incident cases using research criteria among 1344 s Males 284 incident cases 379 Females 95 No incident cases Developmental Medicine & Child Neurology 2006, 48:
3 the records of children from the birth cohort who had received care at the only private community provider of psychiatric care other than the Mayo Clinic or the Olmsted Medical Center and identified four additional potential cases. Finally, in the fifth step, the following explicit, research criteria were applied to identify incident cases among the 1344 possible cases identified in the preceding four steps: (1) symptoms of as specified in DSM-IV (six of nine symptoms of inattention, hyperactivity impulsivity, or both); (2) positive results on questionnaires; and (3) documented clinical diagnoses of. The exclusion criteria specified in DSM-IV were also applied (i.e. participants could not be considered incident cases if they had a diagnosis of pervasive developmental disorder, schizophrenia, or other psychotic disorder). To be designated research-identified incident cases, participants were required to fulfill various combinations of these criteria, as reported previously 6,7 and depicted in Table I. In this birth cohort, 379 children were found to meet research criteria for. Information from the complete medical, psychological, and educational records was ed to identify all children who had completed an individually administered intellectual assessment between 6 and 18 years of age. Children were categorized into three groups: (1) moderate-to-severe intellectual disability (IQ 50); (2) borderline-to-mild intellectual disability (51 IQ 79); and (3) no intellectual disability (IQ 80). For those children who had completed more than one individually administered test of intellectual ability between 6 and 18 years of age, the score obtained at the oldest age was used to place the child into one of the intellectual disability categories. Finally, all children whose educational records did not indicate any concerns about learning or receipt of any special educational services, and who had never had individually administered intelligence testing, were placed into the no intellectual disability category. STATISTICAL ANALYSES The distribution of in children with and without borderline-to-mild intellectual disability was compared by using χ 2 tests. The strength of the association between and borderline-to-mild intellectual disability was estimated by odds ratios (OR) and corresponding 95% confidence intervals (CIs). Statistical analyses were performed with the SAS software package (SAS Institute, Cary, North Carolina). All p values were two-sided, and p values less than 0.05 were considered statistically significant. Results Nineteen of the 5718 children in the birth cohort were found to have moderate-to-severe intellectual disability, defined by a Full-scale IQ 50 or less obtained on an individually administered test of intelligence. These children were not included in the following analyses. Seventy children (39 females, 31 males), representing 1.2% of the birth cohort, were classified as having borderline-to-mild intellectual disability (IQ in the range 51 79). The remaining 5629 children (2710 females, 2919 males) were classified as having no intellectual disability. Of these 5629 children, 1368 had completed individually administered tests of intelligence, and all were given nationally standardized, group-administered achievement tests on a frequent basis, in accordance with the standard policy of the local school district. Of the 70 children classified as having borderline-to-mild intellectual disability, 30% (n=21; 7 females, 14 males) were found to have research-identified. However, of the remaining 5629 children without an intellectual disability, only 6.4% (n=358; 88 females, 270 males) were found to have research-identified. The odds ratio for comorbid research-identified for children with versus without borderline-to-mild intellectual disability was 6.3 (95% CI ; p<0.001). The OR for comorbid research-identified for females with versus without borderline-to-mild intellectual disabilities was 6.5 (95% CI ; p<0.001). Finally, the OR for comorbid research-identified for males with versus without borderline-to-mild intellectual disabilities was 8.1 (95% CI ; p<0.001). We also determined the co-occurrence of research-identified and mild intellectual disability, defined by an IQ between 51 and 69. We identified 19 children (12 females, 7 males), representing 0.3% of the birth cohort, with mild intellectual disability. Of these, 31.6% (n=6; 2 females, 4 male) had research-identified, in comparison with only 6.6% (n=373; 93 females, 280 males) with in children with an IQ 70 or higher. The OR for comorbid research-identified for children with versus without mild intellectual disability was 6.6 (95% CI ; p<0.001). The OR for comorbid research-identified for females with versus without mild intellectual disability was 5.7 (95% CI ; p<0.012). Finally, the OR for comorbid research-identified for males with versus without mild intellectual disability was 12.7 (95% CI ; p<0.001). Although the OR for in males with borderline-to-mild intellectual disability differed from that for females, the relatively small number of participants does not Table I: Research criteria for attention-deficit hyperactivity disorder () case definition cases Meets DSM-IV questionnaire Clinical diagnoses Total nr of participants criteria for a results of Research-identified cases Plus and minus signs indicate the presence or absence respectively, of a given criterion. a All Diagnostic and Statistical Manual of Mental Disorders 4th Edition (DSM-IV) 9 criteria were met, with the exception that age criterion (some symptoms documented before age of 7y) was not used. and Intellectual Disability Robert G Voigt et al. 833
4 permit meaningful statistical comparison by sex. Discussion Our findings indicate that children in this population-based birth cohort with borderline-to-mild intellectual disability were six times more likely to have research-identified as children without intellectual disability. Our results provide evidence to support the neurodevelopmental model for understanding the spectrum of developmental disabilities described by Capute and Accardo. 1 3 More specifically, we have shown that developmental dissociation and/or deviance, as represented by, are more likely to occur in the context of developmental delay, represented by borderline-to-mild intellectual disability. In the past, the symptoms of inattention, hyperactivity, and impulsivity were often considered an attribute of a child s intellectual disability, rather than potentially representing an associated or comorbid condition, or a dual diagnosis. 10 This led to mutually exclusive classification of intellectual disability and. Certainly, both intellectual disability and remain in the differential diagnosis of inattentive behavior. Our data clearly indicate, however, that the symptoms of are not a universal attribute in children with borderline-to-mild intellectual disability. Indeed, 70% of the children in our birth cohort who had borderline-to-mild intellectual disability did not meet our research criteria for. Thus, rather than representing a ubiquitous attribute of children with intellectual disability, our data indicate that can and should be recognized as a common comorbid condition in children with such a cognitive disability. We excluded children with moderate-to-severe intellectual disability (IQ 50) in view of the difficulty in ascertaining the developmental inappropriateness of complaints of inattention or impulsivity in individuals with more severe intellectual disability. However, consistent with the Capute and Accardo neurodevelopmental model, children with more significant intellectual delays are at greater risk not only for hyperactive and disinhibited behaviors but also for increasingly developmentally deviant behavioral manifestations such as aggression, stereotypies, self-injury, and autism. 2,4,10,11 Unfortunately, despite our finding of such a high co-occurrence of and borderline-to-mild intellectual disability, the diagnosis and management of in children with intellectual disability have not been well studied, because the presence of below-average intelligence, defined as an IQ of less than 80, has been an exclusionary criterion in the large majority of studies of in the general population Previous population-based studies of the occurrence of psychiatric disorders in children with intellectual disabilities have reported that hyperactive or hyperkinetic behavior occurs in 9 to 11% of those with borderline-to-mild mental retardation In a more recent study of children with borderline-to-moderate intellectual disability who were attending a special school for the intellectually impaired, 14.8% of the children met DSM-IV symptom criteria for. 18 In comparison with these previous findings, our data, derived from a population-based birth cohort, show a higher rate of in children with borderline-to-mild intellectual disability than previously reported. We found that 30% of children with borderline-to-mild intellectual disability met our research criteria for. Thus, our data suggest that is likely to be significantly under-recognized, and, therefore, undertreated, in children with borderline-to-mild intellectual disability. The potential for under-recognition and undertreatment of is of particular concern given existing evidence for the very effective, but probably underused, treatment of with stimulant medication in children with borderline-to-mild intellectual disability. 14,15 Indeed, it has been reported previously that only 7.5% of children with mild intellectual disability receive stimulant medication. 12,17 In addition, it has recently been shown that, in comparison with children with intellectual disability who do not have, children with intellectual disability and comorbid show more symptoms of depression, family conflict, non-compliance, anxiety, inadequate social skills, and academic problems. 19 Two recent long-term studies of children with intellectual disability and have established the chronicity of symptoms in these children. 20,21 These studies have also shown that children with intellectual disability and comorbid are at increased risk of being suspended from school, having conduct and legal problems, and requiring inpatient psychiatric hospitalizations. Thus, appropriate diagnosis and treatment of in children with borderline to mild intellectual disability is imperative in view of the increased risk for longterm functional impairment, and probably increased health care costs and utilization, 22 compared with children with intellectual disability who do not have. Our study has several potential limitations. First, many individuals in our birth cohort completed formal intelligence testing on several occasions between 6 and 18 years of age. As reported in previous studies, 23 we found variability in these scores over time. However, intelligence test scores obtained at older ages during childhood are more reliable and valid measures of intelligence than scores obtained at younger ages. 24 We, therefore, used intelligence test scores obtained at the oldest age for those children who had multiple evaluations to categorize a participant as having moderate-to-severe, borderline-to-mild, or no intellectual disability. Our study was also limited by the retrospective nature of the data; we did not directly evaluate every child in the birth cohort. We realize that the absolute number of children identified with borderline-to-mild intellectual disability in our birth cohort was lower than expected; however, we have two reasons to assert that we have not failed to identify children with borderline-to-mild intellectual disability in this population. The first is the wealth of accumulated data in our medical and school records: 34% (n=1951) of the 5718 participants in our birth cohort were identified as having school problems, and 25% (n=1457) had IQ scores from individually administered intelligence tests completed between 6 and 18 years of age. This reflects the unusual access to high-quality medical care and educational services in this community. Second, all participants in our birth cohort were given nationally standardized, group-administered achievement tests on a frequent basis in accordance with the standard policy of the local school district. The distribution of scores on achievement testing was shifted to the right, reflected in a median national centile score in reading achievement at the 73rd centile at 12 years of age for participants in our birth cohort. It is, therefore, unlikely that we have underestimated the number of children with borderline-to-mild intellectual disability in our participants. Furthermore, the critical issue for this study was the comparison of occurrence between children with and without intellectual disability in this specific population. Nevertheless, when we studied only the children with mild 834 Developmental Medicine & Child Neurology 2006, 48:
5 intellectual disability, rather than the entire group identified with borderline-to-mild intellectual disability, we found that children with mild intellectual disability (51 IQ 79) were nearly seven times as likely to meet our research criteria for as children without mild intellectual disability. It is also important to recognize that may negatively affect a child s performance on intelligence testing, and this might potentially have affected the intellectual disability classification of some children. For example, the IQ difference between children with and comparison children without has been reported to be as much as 7 to 12 IQ points. 25 Finally, another limitation of our study is that the population of Rochester during 1976 to 1982 was largely Caucasian and fairly homogenous in terms of socioeconomic status, potentially limiting our ability to generalize these results to populations having greater diversity of socioeconomic status and ethnic background. Nevertheless, because of the relative homogeneity of the Rochester population, our birth cohort could be the ideal sample to concentrate on issues of developmental delay, dissociation, and deviance, without having to deal with some of the extremes that will be encountered in other settings. Conclusion In this birth cohort we found that children with borderlineto-mild intellectual disability were significantly more likely to meet our research criteria for than those children without intellectual disability. These data provide evidence for the neurodevelopmental model for understanding the spectrum of developmental disabilities described by Capute and Accardo, because developmental dissociation and/or deviance (represented by in this study) were found to be more likely to occur in the context of developmental delay (represented by borderline-to-mild intellectual disability in this study). Although intellectual disability and are both in the differential diagnosis for clinically significant symptom patterns of inattentive, impulsive, and/or hyperactive behavior, our data indicate that and intellectual disability are common comorbid conditions and should not be considered mutually exclusive. Children with borderline-to-mild intellectual disability should be evaluated for the presence of associated, and appropriate educational, behavioral, and medication interventions specifically aimed at managing the symptoms of should be implemented. Early recognition of and intervention for comorbid in children with borderline-to-mild intellectual disability are likely to enhance academic, social, and vocational skills required for independent living and are, therefore, likely to improve the long-term outcome for these children. DOI: /S Accepted for publication 20th March References 1. Capute AJ, Accardo PJ. (1996) A neurodevelopmental perspective on the continuum of developmental disabilities. In: Capute AJ, Accardo PJ, editors. Developmental Disabilities in Infancy and Childhood. 2nd edn. Baltimore: Paul H Brookes. p Capute AJ. (1991) The expanded Strauss syndrome: MBD revisited. In: Accardo PJ, Blondis TA, Whitman BY, editors. Attention Deficit Disorders and Hyperactivity. New York: Marcel Dekker, Inc. p Capute AJ, Accardo PJ. (1996) The infant neurodevelopmental assessment: a clinical interpretive manual for CAT-CLAMS in the first two years of life, part 1. Curr Probl Pediatr 26: Dykens EM. (2000) Psychopathology in children with intellectual disability. J Child Psychol Psychiatry 41: Melton LJ. (1996) History of the Rochester Epidemiology Project. Mayo Clinic Proc 71: Katusic SK, Barbaresi WJ, Colligan RC, Weaver AL, Leibson CL, Jacobsen SJ. (2005) Case definition in epidemiologic studies of attention-deficit/hyperactivity disorder. Ann Epidemiol 15: Barbaresi WJ, Katusic SK, Colligan RC, Pankratz VS, Weaver AL, Weber KJ, Mrazek DA, Jacobsen S. (2002) How common is attention-deficit/hyperactivity disorder? Incidence in a population-based birth cohort in Rochester, Minnesota. Arch Pediatr Adolesc Med 156: Katusic SK, Colligan RC, Beard CM, O Fallon WM, Bergstralh EJ, Jacobsen SJ, Kurland LT. (1996) Mental retardation in a birth cohort, , Rochester, Minnesota. Am J Ment Retard 100: American Psychiatric Association. (1994) Diagnostic and Statistical Manual of Mental Disorders. 4th edn. Washington, DC: American Psychiatric Association. 10. Lovell RW, Reiss AL. (1993) Dual diagnoses: psychiatric disorders in developmental disabilities. Pediatr Clin North Am 40: Einfeld SL, Tonge BJ. (1996) Population prevalence of psychopathology in children and adolescents with intellectual disability. II. Epidemiological findings. J Intellect Disabil Res 40: Weber P, Lutschg J. (2002) Methylphenidate treatment. Pediatr Neurol 26: Pearson DA, Santos CW, Roache JD, Casat CD, Loveland KA, Lachar D, Lane DM, Faria LP, Cleveland LA. (2003) Treatment effects of methylphenidate on behavioral adjustment in children with mental retardation and. J Am Acad Child Adolesc Psychiatry 42: Pearson DA, Santos CW, Casat CD, Lane DM, Jerger SW, Roache JD, Loveland KA, Lachar D, Faria LP, Payne CD, Cleveland LA. (2004) Treatment effects of methylphenidate on cognitive functioning in children with mental retardation and. J Am Acad Child Adolesc Psychiatry 43: Jacobson JW. (1982) Problem behavior and psychiatric impairment within a developmentally disabled population. I. Behavior frequency. Appl Res Ment Retard 3: Gath GA, Gumley D. (1986) Behaviour problems in retarded children with special reference to Down s syndrome. Br J Psychiatry 149: Gadow KD. (1985) Prevalence and efficacy of stimulant drug use with mentally retarded children and youth. Psychopharmacol Bull 21: Dekker MC, Koot HM. (2003) DSM-IV disorders in children with borderline to moderate intellectual disability: prevalence and impact. J Am Acad Child Adolesc Psychiatry 42: Pearson DA, Lachar D, Loveland KA, Santos CW, Faria LP, Azzam PN, Hentges BA, Cleveland LA. (2000) Patterns of behavioral adjustment and maladjustment in mental retardation: comparison of children with and without. Am J Ment Retard 105: Aman MG, Pejeau C, Osborne P, Rojahn J. (1996) Four-year follow-up of children with low intelligence and. Res Dev Disabil 17: Handen BL, Janosky J, McAuliffe S. (1997) Long-term follow-up of children with mental retardation/borderline intellectual functioning and. J Abnorm Child Psychol 25: Leibson CL, Katusic SK, Barbaresi WJ, Ransom J, O Brien PC. (2001) Use and costs of medical care for children and adolescents with and without attention-deficit/hyperactivity disorder. JAMA 285: McCall RB. (1984) Developmental changes in mental performance: the effect of the birth of a sibling. Child Dev 55: Sattler JM. (2001) Issues related to the measurement and change of intelligence. In: Sattler JM, editor. Assessment of Children: Cognitive Applications. 4th edn. San Diego: Jerome M Sattler, Inc. p Kuntsi J, Eley TC, Taylor A, Hughes C, Asherson P, Caspi A, Moffitt TE. (2004) Co-occurrence of and low IQ has genetic origins. Am J Med Genet B Neuropsychiatr Genet 124: and Intellectual Disability Robert G Voigt et al. 835
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