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This study aimed to investigate the behavioral and motor development of full-term Taiwanese toddlers with ASD, and to compare with full-term TD and VLBW preterm toddlers. The results revealed that the toddlers with ASD exhibited high degrees of various behavioral problems and poor motor functions at ages of 30 and 36 months.

Although VLBW preterm toddlers associate with exhibiting Externalizing problems and poor locomotion skill, their effects on behavioral or motor problems were milder than those of full-term toddlers with ASD. The results provide important insights into understanding of behavioral and motor development in Taiwanese toddlers with ASD, and highlight the need for clinicians to emphasize on early intervention for behavioral and motor developmental problems in toddlers with ASD.

5.1 Behavioral problems in Taiwanese toddlers with ASD

Taiwanese full-term toddlers with ASD exhibited higher behavioral problems scores in most of CBCL/1.5-5 scales compared to the TD toddlers. Our findings were consistent with other studies that young children with ASD aged 1 to 8 years

demonstrated high degrees of aggressive behaviors (Rojahn et al., 2009), inattention and hyperactivity (Mayes, Calhoun, Mayes, & Molitoris, 2012), mood disturbance (Mayes et al., 2012), sleep problems (Mazurek & Sohl, 2016; Souders et al., 2009), and

withdrawn behaviors (Albores-Gallo, Betanzos-Cruz, Santos-Sánchez, Lemus-Espinosa,

& Hilton, 2012; Hartley, Sikora, & McCoy, 2008; Limberg, Gruber, & Noterdaeme, 2016). Furthermore, Narzisi et al. (Narzisi et al., 2013) examined behavioral problems in Italian toddlers with ASD at ages of 18 - 36 months by the CBCL/1.5-5. Their results were similar to our data that Italian toddlers with ASD obtained high degrees of

behavioral problems in all CBCL/1-1.5 scales. The findings highlights the needs that early assessment of associated behavioral problems and syndromes in toddlers with

ASD is important for early intervention.

A prior study by Hartley et al. (Hartley, Sikora, & McCoy, 2008) examined the prevalence of behavioral problems and syndromes using the CBCL/1.5-5 among 169 American toddlers with ASD aged 1.5 - 5.8 years. They found 27% - 34% of cases had high degrees of clinically-ranged Internalizing, Externalizing and Total Problems.

Nevertheless, the rates of clinically-ranged Total Problems (43.3%) and Internalizing Problems (60%) in our study were higher than those in American toddlers with ASD.

Furthermore, the higher syndromes and problems scores were mostly among the Internalizing-related syndromes, especially the Withdrawn syndrome. The findings reflected that core symptoms of ASD such as problems in environmental adaptation, difficulty to express their emotion or thoughts in jointed activities, and

social-communication deficits to show the interests with other people may result in high degrees of internalizing-related problems, and may challenge parents facing more rearing problems in the daily life. Since behavioral problems in 2 to 4-year-old children were relatively higher than the older-aged children, which is called the “Trouble age 2 or 3,” it is not surprising that the rates of Taiwanese toddlers with ASD may exhibit more severe behavioral problems because the ASD symptoms, such as

social-communication deficits, unusual interests and stereotyped behaviors may interfere their behavioral performances. Our findings revealed that more complicated features of behavioral development should be noticed in Taiwanese toddlers with ASD.

A longitudinal follow-up of our ASD sample is necessary if the behavioral problems and syndromes persist into school ages or adolescence.

5.2 Behavioral trajectories and interests in Taiwanese toddlers with ASD

The results of behavioral tracking data revealed that our full-term toddlers with ASD showed more interest to stay in the periphery region, spent less time of latency to

approach parent region, and higher absolute angular velocity of turning movements compared to the full-term TD toddlers. Cohen et al. (Cohen, Gardner, Karmel, & Kim, 2014) have been used the same tracking system and very similar procedures to examine behavioral trajectories and interest in a sample of children with ASD (mean age: 5.8 years). They also found that children with ASD had higher interests to stay in the peripheral region compared with non-ASD toddlers. Previous studies reported that higher degree of autism severity were associated with more severe stereotypies, restricted and repetitive behaviors, and more non-purposed seeking behaviors or self-stimulating behaviors (Ben-Sasson et al., 2009; Cohen et al., 2014; Troyb et al., 2016). Since the periphery region in our study were surrounded by curtains and walls, children with ASD preferred to approach and stay in periphery for seeking more sensory stimuli, such as rub their body against the wall or cover their body with curtains. In addition, we observed that Taiwanese toddlers with ASD tended to perform very simple and stereotyped object-manipulation skills during the behavioral tracking procedures.

For instances, they repetitively throw away the toys and then picked up them again, or knocked toys to floor or wall, or more likely to turn around many times. Our findings revealed that restricted behavioral interests and abnormal turning movements may help to discriminate toddlers with ASD from TD toddlers. The findings suggest that

automated behavioral tracking device is a valid tool that could capture real-time behavioral trajectories of toddlers with ASD and to provide two-dimensional data of measuring child’s interest toward specific region and repetitive turning movements.

5.3 RRBs in Taiwanese toddlers with ASD

Taiwanese toddlers with ASD exhibited higher stereotyped, sameness and restricted behaviors scores assessed by the RBS-R compared to the TD toddlers. The findings were consistent with other studies that children with ASD aged 8 - 71 months

demonstrated larger inventories and higher degrees of repetitive and stereotyped movement (Barber, Wetherby, & Chambers, 2012; Kim & Lord, 2010; Morgan,

Wetherby, & Barber, 2008), insistence to remain sameness, and inflexible adherence to routines or rituals and restricted interest (Fulceri et al., 2016; Richler, Bishop, Kleinke,

& Lord, 2007). However, we found no differences in Self-injured, Compulsive, and Ritualistic behaviors scores between toddlers with ASD and TD toddlers. Our finding was similar to Fulceri et al (Fulceri et al., 2016) that low diagnostic accuracy of ASD (AUC = 0.61-0.68) were found in both Self-injured and Compulsive behaviors scores among the Italian children aged 23 to 71 months. Self-injured behaviors in young children with ASD commonly appeared in toddlers with severe symptoms of ASD that may be caused by serious problems in communicating with people, high levels of frustration, and severe emotional reactivity in avoidance of interaction. A possible explanation is that 14 of 15 toddlers with ASD in our study receive one or more regular developmental interventions per week which may decrease their severities of symptoms of ASD and lead to less self-injured behaviors. In addition, previous studies (Evans et al., 1997; Zohar & Felz, 2001) reported that the amount of compulsive behaviors in TD children reached a high level between 2 - 4 years of age. Since some of our TD toddlers exhibited various and high degrees of compulsive behaviors, this might be a possible reason that no obvious difference between TD toddlers and FT-ASD toddler. In addition, Schertz et al. (Schertz, Odom, Baggett, & Sideris, 2016) have reviewed and compared the RBS-R scores in person with ASD from the early childhood to adulthood (16 months to 51 years of age). The study have reported that the amount of ritualistic behaviors in 5 to 9-year-old children with ASD were higher than other ages of children with ASD. It is necessary to long-term follow up for the ritualistic behaviors in our sample at older ages. Moreover, Radonovich et al. (Radonovich, Fournier, & Hass, 2013)

have reported that older-aged Indian children with ASD (3-16 years of age) obtained significantly higher scores in all RBS-R scales than did the TD toddlers. Therefore, more longitudinal follow-up for evaluating changes of RRBs over time in toddlers with ASD is warranted in the future study.

5.4 Motor developmental problems in Taiwanese toddlers with ASD

Taiwanese toddlers with ASD showed overall poor motor functions as comparing to the motor development in the TD toddlers. Previous studies have reported delayed posture development (Nickel, Thatcher, Keller, Wozniak, & Iverson, 2013; Ozonoff et al., 2008), delayed onset of walking and lack of reciprocal arm movements (Bhat, Landa,

& Galloway, 2011) and poor manual-motor skills (Gernsbacher, Sauer, Geye, Schweigert, & Hill Goldsmith, 2008; Ozonoff et al., 2008) in 6 to 46 month-old

children with ASD. Furthermore, although few studies used standardized developmental assessment instrument for evaluating motor development among toddlers with ASD, Ozonoff et al. (Ozonoff et al., 2014) found some similar results that young children with ASD aged 12 months obtained lower fine motor scores of the MSEL than the TD

children. Our study used the PDMS-2 that includes more items for measurement of motor proficiency in multiple motor subdomains which would be better able to evaluate motor skills in toddlers with ASD. Besides, Provost et al. (Provost, Lopez, & Heimerl, 2007) have used the PDMS-2 to examine the motor development in 19 American toddlers with ASD aged 21 to 41 months, and the results showed high percentages (94.7%) of toddlers were to be classified as below average or poor performance in the Total, Gross and Fine motor Scales of PDMS-2. Comparing to their results, the rates of below average or poor performance in Total (80%) or Fine Motor Scales (73.3%) in our sample were slightly to be lower, but was high in Gross Motor Scale (93.3%). Among 15 toddlers with ASD in our study, we found that only 4 toddler with ASD continuously

receive a pediatric physical therapy which focused on their gross and fine motor developments. Our findings implicated that motor interventions for these toddlers with ASD might be insufficient. The results indicated that the motor development should be noticed in Taiwanese toddlers with ASD and highlight the needs for clinicians to be aware of early identification and intervention for the early motor problems.

In addition to the gross and fine motor development in toddlers with ASD, our data provide further information in the subdomains of motor development. We found that high rates of Taiwanese toddlers with ASD exhibited poor performance in Locomotion (40%), Grasping (26.7%) and Visual-Motor Integration subscales (26.7%), whereas Provost et al. (Provost, Lopez, & Heimerl, 2007) reported poor performance of

Locomotion, Object-Manipulation and Visual-Motor Integration subscales in American toddlers with ASD. The discrepancy that our sample showed poor grasping function may be due to insufficient experiences of drawling pictures that some items tested child’s ability to write/hold a pen. Previous studies proposed that poor motor function in young children with ASD may be associated with the core ASD symptoms of

social-communication dysfunction (Bhat, Galloway, & Landa, 2012; Sipes, Matson, &

Horovitz, 2011) and repetitive and stereotyped movements (Elison et al., 2014;

Radonovich et al., 2013). Toddlers with ASD may decrease the motivations to observe or imitate other peoples’ movements which may result in less motor experiences. For examples, 2 to 3-year-old children normally develop several ball (e.g. throwing,

catching, kicking balls) and locomotion skills (e.g. jumping up/down/forward, jumping hurdles, running, and walking in a line) during outdoor games with peers. However, toddlers with ASD would be more frustrated to keep social attentions and engagement during the activities. Besides, high degrees of RRBs in toddlers with ASD may limit their ability to explore and integrate multiple cues that toddlers with ASD are hard to

complete several motor activities, such as grasping marker, building tower, drawing geometries, folding paper, and stringing beads that needs good ability of visual-motor integration. In addition, our results showed no significant differences in stationary function between toddlers with ASD and TD toddlers. The comparable development may be due to all of our toddlers with ASD could stand and walk independently that would be no obvious problems in the Stationary subscales before 3 years of age. In light of the higher functioning of one-leg standing and complex motor planning develop around 3 years of age, longitudinal follow-up for their long-term motor development is warranted.

5.5 Behavioral and motor developments between full-term toddlers with ASD and VLBW preterm Toddlers

The results revealed that FT-ASD toddlers exhibited higher degree of various CBCL/1.5-5 Scales scores, more RRBs and more restricted behavioral interest in periphery region, and overall lower PDMS-2 motor scores than did FT-TD toddlers, whereas most of behavioral or motor developmental indicators were comparable

between VLBW-PT and FT-TD toddlers. The VLBW-PT toddlers showed higher scores in Sleep Problems, Aggressive Behavior, Externalizing and Total Problems and lower Locomotion scores compared to the TD toddlers. Our data were inconsistent with a prior study that VLBW preterm toddlers may exhibit various behavioral problems and syndromes such as aggressive behaviors, somatic complaints, internalizing,

externalizing problems (Reijneveld et al., 2006) and sleep problems (Stangenes et al., 2017). Mild behavioral or motor developmental problems presented in our VLBW preterm toddlers may be in part due to our study excluded severe perinatal or neonatal diseases for selecting VLBW preterm toddlers. Besides, VLBW-PT toddlers’ behavioral characteristics and interests were similar to those of FT-TD toddlers, except for

VLBW-PT toddlers tended to show a short latency to approach parent. Our findings may be explained that parental overprotection were found to be more likely to appear in VLBW preterm infants and may be associated with poor adaptive behavior skills and less independency while exploring new environment (Wightman et al., 2007). In addition, our findings were inconsistent with previous studies that no differences of RBS-R Scales scores between VLBW-PT and FT-TD toddlers. Our VLBW-PT toddlers did not show any autistic-like symptoms of RRBs may be due to 60% of VLBW preterm toddlers have received a family-centered intervention program from birth to 1 year of age which may have positive effects on their developmental outcomes.

Moreover, several studies have shown that VLBW or EBLW preterm children displayed delayed motor milestones, more impaired gross and fine motor function than the TD children in early childhood (Cahill-Rowley & Rose, 2016; de Kieviet et al., 2009;

Ferrari et al., 2002; Pin et al., 2010; van Haastert et al., 2006). Although our results reported comparable motor scores in most of PDMS-2 Scales between the VLBW-PT and FT-TD toddlers, the VLBW-PT toddler performed lower Locomotion scores than that of FT-TD toddlers. The poor locomotion skills in VLBW preterm toddlers may be due to insufficient muscle strength and endurance that might be hard to display good strategies in some locomotion skills, such as, jumping, running or up/down stairs.

In addition, the results revealed that both FT-ASD toddlers and VLBW-PT toddlers exhibited significantly higher degree of multiple behavioral problems than FT-TD toddlers. However, the adverse effects of ASD on multiple behavioral problems and locomotion problems were greater than the effects of VLBW and preterm birth. The present study is the first study to examine the effects of ASD versus VLBW and preterm birth on toddlers’ behavioral and motor problems. Several studies have compared young children with ASD and ATD children with different developmental problems. Previous

studies have reported that young children with ASD had more behavioral problems and poorer motor development compared to the ATD children. For examples, Narzisi et al.

have found that children with ASD aged of 18 - 36 months obtained significantly higher degree of multiple behavioral problems than did ATD peers. Furthermore, several studies reported that children with ASD aged 12-24 months exhibited more repetitive and stereotyped body movement or use of objects (Elison et al., 2014; Morgan,

Wetherby, & Barber, 2008), more abnormal sensory behaviors (Watt, Wetherby, Barber,

& Morgan, 2008), more compulsions and rituals (Richler, Bishop, Kleinke, & Lord, 2007) compared to developmental delayed toddlers. The reasons that higher degrees of behavioral and motor problems in toddlers with ASD may be due to the complex ASD symptoms that may associate with adverse developmental outcomes. Furthermore, we found that only 6 VLBW preterm toddlers received the diagnosis of global

developmental disorders, language disorders or motor delay, which the overall

behavioral or motor performance might be relatively milder than the toddlers with ASD.

Our findings suggest that full-term toddlers with ASD might associate with more adverse behavioral and motor outcomes as comparing to the VLBW preterm toddlers.

Future study may further examine whether these developmental indicators may differ between the full-term toddlers with ASD and VLBW preterm toddlers with ASD to verify the effects of VLBW and preterm birth.

5.6 Limitation

The present study has some limitations that are important to mention. First of all, although our sample sizes were appropriate to achieve statistical power, varied

spectrums of child’s developmental level in ASD should be noticed because half of toddlers with ASD in our study had very low level of cognition. Whether there is a subgroup effect that ASD combined severe cognitive delay may have different

behavioral or motor development is unknown. Second, our study did not matched for child’s characteristics such as age, sex and social-economic status among the 3 study groups. Although there were no significant differences for subject characteristics among the groups, the matched group design would be better to decrease the influences that the differences of demographic characteristics might affect the results. Third, although the PDMS-2 is a standardized and comprehensive motor tests for assessment of toddlers’

motor functions, our experiences revealed that toddlers with ASD tended to cry, frustrate, or escape during the process of testing. It took a longer time to complete the testing that might interfere the accuracy of testing results because child’s performance may be affected by negative emotions, fatigue and insufficient motivation in children with ASD. Finally, it would be better to recruit the group of VLBW preterm toddlers with ASD that may help to verify the effect of VLBW and preterm birth versus full-term birth on developmental performance among the toddlers with ASD. The current study emphasizes the needs for researchers and clinicians to consider behavioral and motor development in toddlers with ASD at ages of 30 and 36 months.

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