Published online February 1, 2007
PEDIATRICS Vol. 119 No. 2 February 2007, pp. e435-e443 (doi:10.1542/peds.2006-1477)
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ARTICLE

Factors Associated With the Diagnosis of Neurodevelopmental Disorders: A Population-Based Longitudinal Study

Chuan-Yu Chen, PhDa, Chieh-Yu Liu, PhDb, Wen-Chuan Su, MSca, Su-Ling Huang, MSca and Keh-Ming Lin, MD, MPHa

a Divisions of Mental Health and Substance Abuse Research
b Biostatistics and Bioinformatics, National Health Research Institutes, Taipei, Taiwan


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
OBJECTIVES. We investigated the occurrence of newly diagnosed mental retardation, attention-deficit/hyperactivity disorder, and autism and sociodemographic factors associated with their distribution in Taiwan, and we examined urbanicity- and socioeconomic status–associated differences in the age at first diagnosis.

METHODS. The data for this study were derived from the 1996–2004 National Health Insurance Research Database in Taiwan. Approximately 1.8 million beneficiaries born between 1996 and 2001 were identified, with follow-up periods ranging from 3 to 8 years.

RESULTS. Each of the 3 neurodevelopmental disorders had distinct incidence rates and associated factors. For example, as compared with the birth years of 1996–1999, the rate of autism increased 14% during the period 2000–2004, whereas the rate of newly diagnosed mental retardation decreased 42% to 50% over the same period. An elevated incidence rate for attention-deficit/hyperactivity disorder and autism was observed in later birth cohorts. The risk of receiving a diagnosis of mental retardation for children in rural areas and of lower socioeconomic status was reduced in early childhood and increased in school ages as compared with their urban and higher socioeconomic status counterparts.

CONCLUSIONS. Variation in the rate of newly diagnosed mental retardation, attention-deficit/hyperactivity disorder, and autism among children in Taiwan depended on age, birth year, period, and socioeconomic status. The extent of the association linking age with the first diagnosis of mental retardation varies across different urbanicity level and socioeconomic status.

Key Words: mental retardation • autism • attention deficit hyperactivity disorder • epidemiology • and incidence

Abbreviations: ADHD—attention-deficit/hyperactivity disorder • MR—mental retardation • NHIRD—National Health Insurance Research Database • NHIP—National Health Insurance Program • NHI—National Health Insurance • EC—enrollee category • IRR—incidence rate ratio • CI—confidence interval • SES—socioeconomic status

Over the past 2 decades, researchers and practitioners in medicine, public health, education, and social work have shown an ever increasing concern regarding neurodevelopmental disorders.1–3 Neurodevelopmental disorders are characterized by a variety of behavioral, communication, or cognitive problems, such as attention-deficit/hyperactivity disorder (ADHD), autism, and mental retardation (MR). Most such disorders emerge in the early years of one's life, and severe forms of developmental problems usually demand long-term attention and care by family members and multidisciplinary professionals. Therefore, to provide adequate comprehensive services to affected individuals and their families, the need exists to recognize the occurrence of childhood-onset neurodevelopmental disorders and to identify the factors influencing their distribution in the general population.

The descriptive epidemiology of neurodevelopmental disorders is changing over time,4,5 and the pattern of change seems heterogeneous across disease categories. Data from the United Kingdom, United States, and Denmark show that the incidence and prevalence of diagnosed and treated autism and ADHD rose,1,5–12 whereas the prevalence of MR fell in the same period.13–15 Possible reasons for the observed differences in incidence rate have been suggested, including changes in the definition and concept for autism and ADHD over time, improved ascertainment methods, increased availability of medical interventions, and growing awareness and knowledge among parents and professionals.5,7,16,17 However, a bona fide change in incidence is also possible. Factors affecting the distribution of neurodevelopmental disorders include 3 time-associated features (ie, age, period, and cohort), social strata as defined by individual-level factors (eg, gender, socioeconomic status, and educational attainment), and environment-level factors (eg, urbanicity level and geographic characteristics).18–20

Current knowledge of neurodevelopmental disorders comes mainly from North American and European countries.4,11,16,21 Because the occurrence of neurodevelopmental disorders varies markedly between countries or across geographic boundaries,3,5 the lack of disease-specific descriptive epidemiology may lead to a poor understanding of medical, educational, and welfare needs of those affected. This makes health policy and planning difficult or arbitrary. To understand incidence trends of selected major neurodevelopmental disorders and their comparative epidemiology may also raise important questions about the nature of variation in risk factors and medical practice. In this study, we sought to understand time, individual, and environmental characteristics associated with the rate of first diagnosed MR, ADHD, and autism in Taiwan, with a focus on the period of childhood.


   METHODS
TOP
 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Study Population and Sample
The data for this study are from the 1996–2004 National Health Insurance Research Database (NHIRD) in Taiwan.22 The NHIRD, organized and managed by the National Health Research Institutes, is derived from the National Health Insurance Program (NHIP). The NHIP has been implemented since 1995 to provide mandatory comprehensive medical care coverage to all civilian residents in Taiwan. The NHIP coverage rate for those <19 years old was estimated to be 98.7% in 2004, and reasons for nonenrollment included living abroad, missing or untraceable, or simply unable to pay the National Health Insurance (NHI) premiums. The focus of the present study is a subgroup of NHI beneficiaries with birth years 1996–2001. On the basis of birth date in the enrollment data files, a total of 1790966 beneficiaries born between 1996 and 2001 were identified from the NHI research database (1996: n = 329539; 1997: n = 330141; 1998: n = 273140; 1999: n = 287816; 2000: n = 310232; and 2001: n = 260098). Until December 31, 2004, the follow-up period ranged from 3 to 8 years, depending on the birth cohort. This study protocol was reviewed and approved by the Institutional Review Board of National Health Research Institutes.

Assessment and Measures
For each NHI beneficiary, an encrypted unique identification number was used to retrieve his or her medical use records for inpatient service and ambulatory care in the NHI medical claim data files, from birth year to 2004, including medical diagnosis, the date of visit, department of visit, and payment for treatment. The International Classification of Diseases, Ninth Revision, Clinical Modification (1992 edition)23 diagnostic codes for MR (317, 318.0, 318.1, 318.2, and 319), ADHD (314.XX), and autism (299.0X) were used. More than 99.98% of diagnoses for the just-listed neurodevelopmental disorders were retrieved from the NHIP ambulatory care records. The onset of any 1 of 3 neurodevelopmental disorders was defined as the diagnosis code that first appeared in the medical claim records, and the age at diagnosis was determined by subtracting birth date from the corresponding visiting date. In the NHIP, each enrolled child could receive ≥2 diagnoses of neurodevelopmental or genetic disorders simultaneously or consecutively, and the comorbidity rate for the 3 neurodevelopmental disorders under study was estimated to be 15.7%.

Beneficiaries' sociodemographic information regarding age, gender, beneficiary category, and geographic region was obtained from enrollment data files. In addition, to evaluate the associations linking urbanicity level and neurodevelopment disorders, the 359 townships in Taiwan were classified into 3 categories: urban, suburban, and rural areas. The urbanicity classification was based on 5 indices: population density, percentages of residents with college or higher education, percentages of residents >65 years old, percentages of residents who were agriculture workers, and the number of physicians per 100000 people.24 In general, the residents in the urban and suburban areas tended to have a higher socioeconomic status than their counterparts in rural areas.24 Because most of our samples were dependents of the insured (the ones who paid the insurance fee [ie, usually the child's parents, grandparents, or social welfare institution]), the present study used enrollee category (EC) as a proxy measure of SES to classify children into 4 subgroups: EC 1 (eg, civil servants, full-time or regularly paid personnel in governmental agencies and public schools), EC 2 (employees of privately owned enterprises or institutions), EC 3 (self-employed, other employees or paid personnel, and members of the farmers or fishers associations), and EC 4 (substitute service draftees, members of low-income families, and veterans). On average, the payroll-related amount for the health insurance was highest for EC 1, followed by EC 2, EC 3, and EC 4. Before the year of 2000, the NHIP used a different system to reimburse medical claims, called the "A code." To assess possible period effect on medical practice and reimbursement policy (ie, a shift from a 2- to a single-reimbursement coding system in the NHIP from the year 2000 onward), timing of diagnosis was dichotomized as 1996–1999 vs 2000–2004.

Statistical Analysis
Cross-tabulations were first conducted to analyze the distribution of sociodemographic background and cumulative incidence of MR, ADHD, and autism for young beneficiaries, stratified by birth year. For each of 6 birth cohorts under study, estimated age-specific incidence rates for the 3 neurodevelopmental disorders were calculated separately on the basis of the number of newly diagnosed cases and person years at risk at midyear at each age stratum.

Because of the relatively lower occurrence rates and possible variation in incidence over time over the developmental period under study, we turned to the generalized linear models in Poisson distribution with robust variance estimation. Data were first regrouped into different categories on the basis of selected social factors thought to influence the onset of neurodevelopmental disorders. Adjusted incidence rate ratio (IRR) and 95% confidence intervals (CIs) for the occurrence of first-diagnosed MR, ADHD, and autism were obtained by log (base e)–transformed values of slope estimates.25,26 To probe whether the age at first diagnosis of neurodevelopmental disorders is homogeneously distributed across different strata of urbanicity and socioeconomic status (SES), product terms of urbanicity x age and SES x age were added into the models separately, and the statistical significance for the product terms was judged by the conventional P value of .05. All of the data preparation and statistical analyses were conducted using SAS 9.13 (SAS Institute, Cary, NC) and Stata 8.02 (Stata Corp, College Station, TX).27,28


   RESULTS
TOP
 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
On the basis of the most recently released NHIRD in 2004, the observation period ranged from 3 to 8 years. In general, the male population was slightly larger than the female one, and approximately half of the children were covered by the insured with beneficiary category of EC 2. In the oldest birth cohort, the cumulative incidence up to age 8 was 1.29% for MR, 2.69% for ADHD, and 0.34% for autism (Table 1).


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  		TABLE 1 Selected Characteristics for NHI Enrollees With Birth Years 1996–2001, Taiwan

 
Figure 1 depicts the incidence rate for each of 3 neurodevelopmental disorders from birth to age 8 years, with stratification by birth cohort. In general, the pattern of incidence rates seems to vary by disorder. For example, there seems to be cohort differences in the incidence rate of MR and 2 incidence peaks in the older birth cohorts (ie, those with birth years of 1996–1998) as compared with a gradual escalation of incidence for the other 3 younger birth cohorts. Over the same period, the age-specific incidence rates of ADHD were somewhat homogeneous across birth cohorts. The incidence of ADHD rises steadily until age 6 years (eg, 0.97% at age 6 years for cohort members born in 1997), whereas the incidence rate of first-diagnosed autism peaks around age 2 to 3 years and drops gradually from age 4 years to school age.


Figure 1
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  		FIGURE 1 Age-specific incidence rates of MR, ADHD, and autism in childhood, according to birth year, in Taiwan.

 
With statistical adjustment for covariates listed, an elevated incidence rate for ADHD and autism for later birth cohorts was found (Table 2). Children born in 2001 had an approximately twofold to threefold higher risk of receiving a diagnosis of ADHD or autism as compared with their counterparts born in 1996. As to age, the adjusted IRR was highest at age 6 years for MR (IRR: 4.6; 95% CI: 4.16–5.10; P < .001), and the corresponding peak ages for ADHD and autism were 6 years (IRR: 161; 95% CI: 134.8–192.4; P < .001) and 2 years (IRR: 100; 95% CI: 64.3–155.5; P < .001), respectively. As compared with the years before calendar year 2000, the occurrence rate of MR was nearly 42% to 50% lower during the period of 2000–2004, whereas an increase of 3% to 27% was found in autism over the same period.


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  		TABLE 2 Estimated Adjusted IRR for the Onset of Neurodevelopmental Disorders Among Birth Cohorts of 1996–2001 in Taiwan

 
Children in EC 3 and EC 4 were more likely to have had a diagnosis of MR (EC 3: IRR: 1.21; EC 4: IRR: 1.35) but less likely to have received a diagnosis of autism (EC 3: IRR: 0.58; EC 4: IRR: 0.57). Children with health insurance registered in suburban and rural areas were less likely than their peers in urban areas to have a diagnosed neurodevelopmental disorder, and the incidence rate was even 44% lower for ADHD among youngsters enrolled in rural areas (IRR: 0.56; 95% CI: 0.54–0.58; P < .001).

With statistical adjustment for birth cohort, period, gender, EC, region, and urbanicity, urbanicity- and EC-associated differences in the link between age and the diagnosis of neurodevelopmental disorders were only found for MR (most P values for product terms <.05). The urbanicity-level specific adjusted IRR across different age strata, derived from the main effect of urbanicity with the product term of urbanicity x age, are plotted in Fig 2 (top), and similar procedures were performed to produce SES-specific adjusted IRR estimates (Fig 2, bottom). In general, the incidence rate of diagnosed MR for children who had their NHI registered in suburban and rural areas was significantly lower than that of the urban children before age 4 years (eg, at age 3, rural: IRR: 0.83; 95% CI: 0.72–0.95). However, once attaining school ages, the incidence rate of MR for children in suburban and rural areas was elevated ~20% to 50% as compared with their agemates in urban areas (eg, at age 7 years, rural: IRR: 1.46; 95% CI: 1.19–1.78).


Figure 2
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  		FIGURE 2 Estimated adjusted IRR and 95% CIs for the first diagnosis of MR among children, according to urbanicity and EC, in Taiwan in 1996–2004.

 

   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
On the basis of a population-based cohort study with 3- to 8-year follow-up, the present analyses show the rate of first-diagnosed MR, ADHD, and autism, as well as factors influencing the age at receiving a diagnosis of neurodevelopmental disorders in Taiwan. Children with later birth years had higher rates of ADHD and autism, whereas their risk of diagnosed MR seems significantly decreased in the first years of the 21st century. The age-associated risk for MR depended on urbanicity and SES: the more rural and the lower SES that the enrolled children are in, the greater is their chance of receiving the diagnosis of MR at school ages.

Some potential limitations of this study should be considered before more detailed discussion. One limitation was that the diagnosis of neurodevelopmental disorders was obtained solely from 1 source (ie, the NHIP). To the extent that not all enrolled children with neurodevelopmental disorders seek medical professional help or care and the help-seeking process of parents or primary caregivers may depend on their background, this data set may underestimate the incidence and prevalence of MR, ADHD, and autism in childhood, and the level of underestimation is unlikely to be homogeneous for all social strata. Similar problems may also distort the association estimates linking SES (ie, EC) with the first diagnosis of neurodevelopmental disorders. However, the complexity of the reasons for NHIP nonenrollment (eg, staying abroad and unable to pay the premiums) made it difficult to predict the direction of association bias. As multiple-source methods have been recommended to ascertain cases of childhood-onset developmental disabilities,29 future efforts may include collecting data from >1 government or private agencies to obtain more accurate incidence estimates for childhood-onset neurodevelopmental disorders.30

A second limitation of the study is geographic discrepancy between location of health insurance enrollment and actual residential region. For instance, it is not uncommon that the child (beneficiary) is raised by someone living in the southern or eastern rural regions (eg, grandparents) but is the offspring of an insured parent (the one who pays the insurance fee) employed in the northern urban region. Further analyses showed that 80% to 90% of diagnoses of enrolled rural children were made by the hospitals located in the urban and suburban regions of Taiwan, and the urban-located hospitals contributed more than half of the diagnoses for the enrolled suburban children (data not shown here). It is not clear whether the urban-associated excess in diagnoses was the result of limited access to psychiatric and pediatric services in rural areas, misclassification of the enrolled children's residential regions, or a mix of the 2 processes.

Third, we also lacked direct evidence regarding clinical validity of diagnoses for a neurodevelopmental disorder. However, validity should be relatively satisfactory given that the vast majority of MR, ADHD, and autism was first diagnosed in general hospitals (including academic medical centers, metropolitan hospitals, and local community hospitals), in which extensive genetic, psychological, cognitive, or developmental evaluations are done before trained specialists in psychiatry or pediatrics make those diagnoses. Finally, the inherently place-specific data source may impose a slight limitation and hinder the generalizability of results to regions, countries, or societies that exhibit differences in the profiles in population characteristics across urbanicity levels, the diagnostic system for neurodevelopmental disorders, health service delivery systems, and health insurance policies.

The present study has several strengths. Most notably, this research is one of the few population-based studies that collected diagnostic information of neurodevelopmental disorders prospectively from birth onward. The data we obtained are considerably comprehensive for 3 disorders under study because the coverage rate for children in Taiwan is >99%, and 99% of general hospitals had contracts with the NHIP over the study period. Moreover, given that the incidence of neurodevelopmental disorders is particularly rare in childhood (<0.1%), the large nationally representative sample makes it possible to clarify possible age-, period-, and birth cohort-associated differences in the occurrence of MR, ADHD, and autism, taking into account other individual- and environment-level characteristics. Finally, our study is unique in that, by looking at the pattern of 3 early onset neurodevelopmental disorders simultaneously, we were allowed to provide comparative epidemiology in the same historical and environmental context.

In accordance with the literature,4,20,31 our results indicate that preschool boys have approximately twofold to fourfold higher risks of neurodevelopmental disorders than their girl counterparts. Given the nature of this data set (eg, reimbursement for medical services), this observed male excess might be a mixed product of gender differences in incidence rate, help seeking, and referral process.32–34 Nevertheless, our male-associated risk estimates all fall within the ranges reported in previous research from other countries, and subsidiary analyses have shown that this male-related excess was consistent across strata defined by age, urbanicity, and SES (data not shown here). As to onset age, the peaks at first diagnosis for autism and ADHD are consistent with available evidence,35 whereas bimodal distribution was found for MR among earlier birth cohorts. A possible explanation is that the follow-up period is too short for the cohort members with later birth years in the present study to reach school age, a period when developmental problems are more likely to be identified by school teachers.36 This is especially plausible for children who have not attended day care or kindergarten or who had mild MR that was undetected because less cognitive abilities or adaptive skills were demanded in the preschool environment.

Only a few studies have examined the occurrence of multiple neurodevelopmental disorders over time, and the majority produced prevalence estimates exclusively.11,16,21 Among them was 1 study that analyzed administrative data derived from a birth cohort of 1987–1994, indicating that the prevalence of MR in California went down, whereas that of autism rose.16,21 In contrast to the California study, which reported birth cohort-associated differences in age on entry into the service delivery system, the incidence rate of autism in our study peaked uniformly at age 2 to 3 years across 6 birth cohorts. Moreover, contrary to the observation that the incidence of autism leveled off among boys in the United Kingdom during the period 2000–2004,35 we found a significant rising trend among later-born children. Given that the size of period effect is much greater on MR than on autism, some unmeasured confounders may possibly account for the recent decline in newly diagnosed MR, such as the availability of medical intervention.12

The strong inverse associations among urbanicity, region, and EC with the first diagnosis of neurodevelopmental disorders in childhood suggest possible microenvironment and macroenvironment-associated health disparities. Given a lower density of general hospitals and the lack of trained specialists in psychiatry or pediatrics, the suburban or rural areas may fall short in children's general and mental health services. In addition, although Taiwan's compulsory primary education starts at age 6 years, preschool or kindergarten education attendance was very common for children residing in urban areas or coming from higher socioeconomic background. Hence, developmental problems in children who were raised in disadvantaged backgrounds may be at higher risk of being underrecognized or underdiagnosed because of limited access to medical services,37 the parents or primary caregivers' inability to recognize early signs of neurodevelopmental disorders, or restricted or no opportunity for neurodevelopmental disorder detection in places outside the home (eg, day care, school, and after-school programs). However, the present study cannot rule out the possibility that children raised in urban environments may be more likely to be exposed to psychosocial or environmental factors associated with neurodevelopmental disorders.

The significant age-associated variation in the link between urbanicity and EC (ie, only for the first diagnosis of MR but not for autism and ADHD) may indicate that urbanicity and SES differentially affect these 3 disorders. The observed rural- or suburban-associated excess in MR during the first years of primary education may merely reflect underdetection of MR in preschool-age children. It is also possible that the etiologic processes of MR in preschool-age children are different from those in school children. For example, the earlier-onset MR may be primarily attributable to biological or congenital factors (eg, genetics or pregnancy exposure), whereas the later-onset MR may be a result of psychosocial or acquired factors (eg, socioeconomic deprivation or accidents).31,38


   CONCLUSIONS
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
In this population-based study of a nationally representative sample, the occurrence of newly diagnosed MR, ADHD, and autism has changed over the past few years in Taiwan, and the age-related risk for first diagnosis of MR was shown to differ between subgroups defined by urbanicity and SES. Our findings may reinforce the attentions of the pediatricians, child psychiatrists, and general practitioners toward an increasing number of help-seeking families with children of autism or ADHD. To address issues of unmet needs for child mental health services in nonurban areas, a policy of differential reimbursement based on level of urbanicity can be adopted by the NHIP to better allocate limited resources. Also, special programs for clinics or local community hospitals can encourage primary care providers to get advanced training relevant to neurodevelopmental disorders or to provide more opportunities for neurodevelopmental disorders screening. Special education programs to parents or primary caregivers (eg, offered in infant and toddler preventive services), particularly targeting disadvantaged families, may increase recognition and awareness about the early signs of neurodevelopmental disorders. Future research incorporating representative cases of MR with comprehensive evaluation of clinical manifestation and exhaustive assessment of macroenvironmental- and microenvironmental-level risk factors from birth onward will be needed to investigate possible mechanisms or processes contributing to the observed geographic and socioeconomic disparities in child health care.


   ACKNOWLEDGMENTS
 
This work has been supported by the National Health Research Institutes.

We give special thanks to the team in the National Health Research Institutes Department of Research Resource responsible for managing the NHIRD.


   FOOTNOTES
 
Accepted Aug 24, 2006.

Address correspondence to Chuan-Yu Chen, PhD, National Health Research Institutes, Division of Mental Health and Substance Abuse Research, Floor 5, Campus 2, No. 309, Sung-Te Road, Taipei 110, Taiwan. E-mail: cychen{at}nhri.org.tw

The authors have indicated they have no financial relationships relevant to this article to disclose.


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PEDIATRICS (ISSN 1098-4275). ©2007 by the American Academy of Pediatrics

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