A Comparison of the Autistic Behavior Checklist and the Childhood Autism Rating Scale for Suspected Autism in a Large Chinese Sample

Autism is the most common clinical developmental disorder in children. The Childhood Autism Rating Scale (CARS) and Autistic Behavior Checklist (ABC) are the most commonly used assessment scales for diagnosing autism. The aim of this study is to compare the diagnostic validities of CARS and ABC based on a large Chinese sample. A total of 474 children with suspected autism spectrum disorder (ASD) were screened by CARS and ABC. Receiver operating characteristic (ROC) curve analysis was performed and it showed that the area-under-the-curve values of CARS is higher than ABC signicantly (p < 0.05) and the suggested cutoff values of CARS and ABC were 34 and 67, respectively. It indicated that CARS is superior to ABC in the Chinese population with suspected ASD.


Introduction
Autism is a neurodevelopmental disorder that occurs early in childhood, which results in stereotypical interests, communication de cits, social de cits and repetitive behaviors [1]. Autism spectrum disorder (ASD) has recently received more and more attention, as there have been increasing numbers of young children going to mental health services and community child health centers for screening of ASD in China [2]. Moreover, early diagnosis and intervention play a critical role in the treatment of ASD patients [3]. However, the current approach for the diagnosis of ASD was mainly based on the clinical assessments [4][5][6]. The scales most commonly used to diagnose ASD in children are the Autism Behavior Checklist (ABC) and Childhood Autism Rating Scale (CARS) [7].
There are numerous suspected ASD cases (showing one or more symptoms of ASD but no nal diagnosis) that originate from community health-service centers and preschools in China, most of whom are initially screened via the Clancy Autism Behavior Scale (CABS) [8]. The cutoff points 14 of CABS was always used as the criteria of suspected ASD in China. When a suspected ASD case was identi ed, his or her parents will receive the suggestions of going to a hospital for a nal diagnosis. When they get to the hospitals for nal diagnoses, most of them might undergo further assessments such as ABC or CARS.
According to previous studies on various assessments of ASD, CARS exhibits better diagnostic validation compared with that of ABC [9]. However, the diagnostic validations and the corresponding cut-offs for CARS and ABC on individuals with suspected ASD were still unclear [4]. Furthermore, for the suspected ASD in China, it remains unclear as to whether CARS is still a better diagnostic tool than ABC. Furthermore, it is unclear whether the current cut-off points for ABC and CARS are suitable for the accurate diagnosis of ASD.
Therefore, the purpose of this study was to compare the diagnostic validities of CARS and ABC for suspected ASD, as well as to obtain more updated and appropriate cut-off scores for each assessment scale. For the de nition of suspected ASD, we still used the CABS as a screening tool with a cut-off score of 14[8]. A receiver operating characteristic (ROC) curve was used to compare the diagnostic validities of CARS and ABC, as well as the corresponding cut-off determinations. Our present ndings would provide insights into the usage of optimal assessment scales for suspected ASD in Chinese metal health hospitals.

Participants
A total of 591 children outpatients from the ASD Unit at Beijing Children's Hospital between June to November of 2019 were identi ed. There were 474 suspected ASD cases screened with a CABS total score of > 14 points (Exclusion N = 117). The Diagnostic and Statistical Manual of Mental Disorders, Five Version (DSM-5) was used to con rm the diagnosis of ASD via child psychiatrists. Ultimately, a total of 399 children were diagnosed with ASD (Fig. 1). The total sample size included 407 males and 67 females who aged 18 months to 14 years (4.1 ± 1.93). Then, each included suspected ASD was evaluated by CARS and the ABC.

Assessment scales
CARS is one of the most widely used autism assessment scales [10]. It is suitable for children over 18 months old and exhibits good reliability and validity. It is a clinician-rated questionnaire with four frequency levels from 1 to 4 on the basis of observations of individuals and their corresponding information, such as teacher and/or parents reports [11]. CARS is a behavioral rating scale, consisting of 15 items, that is invariably used to quantitatively describe the severity of suspected ASD symptoms [12].
According to the CARS manual, ASD is de ned as a CARS score of ≥ 30 points. A score of 30 or more strongly indicates the existence of ASD. A score of 30-36 suggests mild symptoms, whereas a score of 37 or above suggests moderate to severe ASD [13].
ABC is a well-established assessment scale for screening and diagnosing ASD [7], and it has been used successfully in the differential diagnosis of ASD [14]. The ABC scale contains 57 items segmented into ve categories: social and self-help, body and object use, relating to others, language, and sensory features [15]. On the basis of the degree of association with pathological behavior, each item is rated four frequency levels from 1 to 4. Calculation of the scores for each of the ve domains yields the partial and overall scores for each domain [16]. Based on the sum of these scores, severe behavioral characteristics can then be analyzed. Higher scores indicate more autistic behavioral symptoms, In the present study, we used 68 as the ABC cut-off score since this value has been previously recommended by Krug et al. [14].
In addition, CABS is the most commonly used screening tool on the Chinese mainland [17]. For this assessment scale, parents complete the Chinese version of CABS, which is based on its rst edition in 1969 [17]. A total of 14 items are included, each of which has three frequency levels: "Never'' (score of 0), ''Occasionally'' (score of 1), and ''Frequently'' (score of 2)[8]. In the present study, any participant with a total CABS score ≥ 14 was identi ed as a suspected ASD case.

Statistical analysis
The present study used the statistical package, MedCalc19.0, for all statistical analysis. We primarily used ROC curve analysis to determine the best cut-off values for CARS and ABC and to evaluate the sensitivities, speci cities, and accuracies of CARS and ABC [10]. ROC curve analysis was also used for comparing diagnostic validations. We also calculated the area under the curve (AUC) for both CARS and ABC. Larger AUCs were indicative of improved prediction e cacies. Each cut-off point and its corresponding sensitivity and speci city were also calculated. A p-value < 0.05 was considered to be statistically signi cant.

Ethical approval
The ethics committees of Capital Medical University and BeijingChildren's Hospital authorized the protocols used in the present study. All of the guardians of the participants offered written informed consent. The most commonly applied measure of scale reliability is the Cronbach's alpha coe cient (α), originally developed by Cronbach (1951), which is used for estimating internal consistency [18]. For this coe cient, larger α values (namely those greater than 0.7) are indicative of higher reliability. We found that the Cronbach alpha coe cients of CARS and ABC were 0.772 and 0.426, respectively (Table 1). Therefore, it suggested that the reliability of CARS was higher than that of ABC. In addition, we found that the correlation between CARS and CABS was 0.732.

Results
Next, we performed ROC curve analysis for CARS and ABC, which yielded AUC values of 0.846 and 0.768, respectively (Fig. 2). Notably, ROC curves (AUCs) represent the most commonly applied global index of diagnostic accuracy. The diagnostic capacity of an assessment tool is usually not evaluated by a single number but is instead usually assessed via two or more diagnostic procedures [19]. Diagnosis is generally based on a cut-off or threshold value [20]. It is often recommended that the Youden index be used to de ne the best cut-off point [20]. The cut-off value, which is associated with the maximum of the Youden index, is usually applied as a decision threshold [21]. Table 2 shows the cut-off scores for ABC and CARS with their corresponding sensitivity and speci city values. The results showed that the differences in AUC values and speci cities between CARS and ABC were statistically signi cant (P < 0.05). The false-positive rate (1-speci city) was indicative of a lower misdiagnosis rate [19]. We found that the cut-off values of CARS and ABC were 34 and 67, respectively. More details see the Table 2 and Fig. 2.
The negative predictive values (NPVs) and positive predictive value (PPVs) of CARS and ABC are shown in Table 3. The PPV for ASD of a screening test is de ned as the proportion of children screened as positive who received an ASD diagnosis divided by the total number of screen-positive cases. PPVs and NPVs are affected by the speci city and sensitivity of the screening tool, as well as by the baseline prevalence of ASD in the population being screened [3]. Moreover, we performed a chi-square test on the PPV and NPV values of ABC and CARS, which revealed that there was no signi cant difference identi ed between CARS and ABC.
Based on these results, we suggested the diagnostic procedures for suspected ASD was as follow:

Discussion
In this study, we found that the AUC of CARS was larger than that of ABC. This nding suggests that CARS is better than ABC in terms of its diagnostic validity for suspected ASD. We also found that the cutoff scores of CARS and ABC for suspected ASD were 34 and 67, respectively. Sensitivity and speci city values included in criterion-validity measures are known to be particularly helpful in clinical settings [22].
The results of a t-test on the speci cities between these two assessments also revealed a signi cant difference, indicating that the speci city of CARS was higher than that of ABC. Furthermore, we veri ed that the Cronbach alpha coe cient of CARS was 0.772, while that of ABC was 0.426. This nding suggests that CARS may be more suitable for diagnosing suspected ASD.
CARS is one of the most important tools for the assessment of ASD, such that both clinical and research practices often use it [23]. Recently, CARS-2 was exploited based on the original edition of CARS [24]. CARS-2 (normalized form) is the same as original CARS, whereas CARS-2-HF (high-functioning form) is a newly developed optional diagnostic for evaluating ASD in children over a certain age and with IQ scores above 80 [25]. In this study, we revisited the validation of CARS and found that it functioned as a better diagnostic compared with that of ABC. We also identi ed an updated cut-off score of CARS for its further usage in diagnosing suspected ASD.
One of the advantages of our study is the introduction of the concept of suspected ASD, which differs from concepts offered in previous studies. In China, there are an increasing number of suspected ASD that have been identi ed at community health-service centers and preschools [17]. It has been reported that early diagnosis plays a critical role for improving outcomes of ASD [26]. In this context, preliminary screening tools are a critical step for timely diagnosis and intervention of ASD [27]. As a preliminary screening tool, CABS can help childcare physicians, teachers, and parents to quickly screen children with suspected autism[8].
Moreover, most children with suspected ABC require further assessments, such as via ABC and/or CARS. Based on the results of our present study, we suggest that CARS may be su cient for further assessment of suspected ASD.
Previous studies have suggested that the cut-off scores of CARS and ABC for distinguishing autism and non-autism are 30 and 68, respectively [13,14]. However, for patients with suspected ASD, it has been suggested that these previously proposed cut-off values may no longer be accurate. Based on the results of the present study, we suggest new cut-off value of CARS (namely, a score of 34) for the diagnosis of suspected ASD. Based on our present ndings, we suggest that children with suspected ASD be initially screened via CABS and that any suspected cases be further con rmed via CARS.
Based on clinically suspected children with ASD in this present study, we found that the diagnostic validation of CRAS was better than that of ABC. Although previous studies have con rmed the strength of CARS, the sample sizes have been limited [8]. In the present study, we con rmed that CARS may be more suitable than ABC for diagnosing ASD in China, especially for suspected ASD [28].
The only available means of ASD diagnosis are behavioral assessments rather than blood tests or noninvasive assessments [29]. Furthermore, in order to conduct the most comprehensive evaluation of ASD, different measurement tools are required in different assessment environments. CARS is a valid and reliable assessment tool that is used for diagnosis and screening ASD in a number of countries [30]. As mentioned above, the main purpose of this study was to explore the diagnostic validation of CARS in a large Chinese sample. Our results further con rmed that CARS is able to effectively and e ciently diagnose patients with suspected ASD. Therefore, in order to comprehensively evaluate ASD, we recommend the combined use of CABS and CARS which might improve the e ciency of clinical works in hospitals.
Our study had two speci c limitations: rst, the age range of included parents was large (aged 1.5-14 years), future studies should clarify the diagnosis validation of ABC and CARS in different age groups. Second, CARS is a clinician-based rating scale, whereas ABC and CABS are both self-rating scales [25,31]. Due to some parents being reluctant to face the fact that their children might have ASD, this caveat may have affected the nal ABC and CABS scores associated with this study.

5.conclusion
This study demonstrated that CARS was superior to ABC in terms of its diagnostic validity of assessing suspected ASD cases in children. In the clinical evaluation for suspected ASD, our ndings suggest that the cut-off values of CARS and ABC were 34 and 67, respectively. Based on our results, we recommend the CARS could be used for the assessments for suspected ASD cases in Chinses hospitals.

Declarations
Ethics approval and consent to participate This study was approved and monitored by the by the Ethics Committee of Beijing Children's Hospital.
Written informed consent will be obtained from the participant and/or their guardian before they were included in this study.

Consent for publication
Not applicable.

Availability of data and materials
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Competing interests
All of the authors declare that they have no competing interests.

Funding
This study is supported by the Special Fund of the Pediatric Medical Coordinated Development Center of Beijing Hospitals Authority, No. XTYB201802. Yonghua Cui was the Founder. The funding body had no further role in the study design, the collection, analysis, and interpretation of data, the writing of the manuscript and the decision to submit the paper for publication.

Authors' contributions
For this manuscript, YC took the initiative. FB, YL and RY will participated in the data collection. YL performed the data analysis and JC nished the draft. All authors have read and approved the manuscript.

Figure 1
Flowchart of the recruitment of participants in the present study  The suggested diagnostic procedures of suspected ASD

Supplementary Files
This is a list of supplementary les associated with this preprint. Click to download. Data.xlsx