Early Neurodevelopmental Assessments of Neonates Discharged From the Neonatal Intensive Care Unit: A Physiatrist’s Perspective

Neurodevelopmental Assessments of NICU Graduates

Article information

Ann Rehabil Med. 2023;47(3):147-161

Publication date (electronic) : 2023 June 27

¹Department of Rehabilitation Medicine, Seoul National University Hospital, Seoul National University College of Medicine, Seoul, Korea

²Department of Physical and Rehabilitation Medicine, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea

³Department of Rehabilitation Medicine, St. Vincent’s Hospital, College of Medicine, The Catholic University of Korea, Seoul, Korea

⁴Department of Rehabilitation Medicine, Pusan National University Hospital, Pusan National University School of Medicine-Biomedical Research Institute, Busan, Korea

⁵Department of Physical and Rehabilitation Medicine, Chungnam National University College of Medicine, Daejeon, Korea

⁶Department of Physical and Rehabilitation Medicine, PURME foundation NEXON Children’s Rehabilitation Hospital, Seoul, Korea

⁷Department of Rehabilitation Medicine, Konkuk University Medical Center, Seoul, Korea

⁸Department of Rehabilitation Medicine, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea

⁹Department of Rehabilitation Medicine, Yongin Severance Hospital, Yonsei University College of Medicine, Yongin, Korea

¹⁰Department of Physical and Rehabilitation Medicine, Chonnam National University Hospital, Chonnam National University Medical School, Gwangju, Korea

¹¹Department of Rehabilitation Medicine, Seoul Rehabilitation Hospital, Seoul, Korea

¹²Department of Rehabilitation Medicine, Eunpyeong St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, Seoul, Korea

¹³Department of Rehabilitation Medicine, Dongguk University College of Medicine, Goyang, Korea

Correspondence: Bum Sun Kwon Department of Rehabilitation Medicine, Dongguk University College of Medicine, 27 Dongguk-ro, Ilsandong-gu, Goyang 10326, Korea. Tel: +82-31-961-7460 Fax: +82-31-961-7488 E-mail: bskwon@dumc.or.kr

Received 2023 March 18; Revised 2023 May 16; Accepted 2023 May 26.

Abstract

The survival rate of children admitted in the neonatal intensive care unit (NICU) after birth is on the increase; hence, proper evaluation and care of their neurodevelopment has become an important issue. Neurodevelopmental assessments of individual domains regarding motor, language, cognition, and sensory perception are crucial in planning prompt interventions for neonates requiring immediate support and rehabilitation treatment. These assessments are essential for identifying areas of weakness and designing targeted interventions to improve future functional outcomes and the quality of lives for both the infants and their families. However, initial stratification of risk to select those who are in danger of neurodevelopmental disorders is also important in terms of cost-effectiveness. Efficient and robust functional evaluations to recognize early signs of developmental disorders will help NICU graduates receive interventions and enhance functional capabilities if needed. Several age-dependent, domain-specific neurodevelopmental assessment tools are available; therefore, this review summarizes the characteristics of these tools and aims to develop multidimensional, standardized, and regular follow-up plans for NICU graduates in Korea.

Keywords: Low birth weight infant; Neonatal intensive care unit; Neurodevelopmental disorder; Premature birth; Rehabilitation

INTRODUCTION

Recent advances in neonatal care have led to an increase in the survival rates of preterm infants or those with low birth weight in Korea [1]. The average birth weight is declining, and the incidence of preterm births is on the increase [1,2]. Because preterm or low birth weight infants are at high risk of developmental delays or disorders, early and regular assessments of neurodevelopmental outcomes of graduates of neonatal intensive care units (NICUs) should continue immediately after discharge [3]. However, there is significant heterogeneity in the neurodevelopmental assessment follow-up policies in different countries [4]. A variety of development assessment tools are available for each domain and age range; however, a consensus gold standard is still lacking in terms of defining the best neurodevelopmental assessment and follow-up program for the early diagnosis of developmental delay [5,6].

Early identification of infants at high risk of developmental delays or disorders is critical for timely referral for appropriate intervention and family counseling. Proper surveillance of neurodevelopmental outcomes of infants is necessary due to the following: (1) early detection or diagnosis of developmental delay or neurodevelopmental disorders; (2) timely intervention and provision of individualized care within critical periods for better outcomes; (3) to educate family/caregivers regarding the developmental status, prognosis, and any possible problems or dangers of infants to prevent further deterioration; and (4) to improve functional outcomes of these infants and the well-being and quality of life of the entire family. Earlier involvement of parents in the care of babies with neurodevelopmental impairments before hospital discharge from the NICU is known to be effective in improving the parent-infant relationship, providing a nurturing environment, and targeting the intervention for individualized infant and family needs [7]. There should be sufficient parental education on useful and safe home exercises or play, information on proper feeding, positioning, sleep, and any available social services. In the future, these developmental interventions beyond the NICU should be updated with evidence-based intervention techniques for individual diagnoses.

Regular hospital visits for neurodevelopmental assessments after NICU discharge is widely acknowledged; however, there should be a systematic follow-up program for both appropriate diagnosis of neurodevelopmental delay and assessment of the efficacy of developmental interventions [5]. Developmental surveillance programs for NICU graduates should include all domains of neurological, motor, language, cognition, perception, and social skills. Moreover, this program should be encouraged to consider each child’s developmental status, caregiver’s socioeconomic status, individualized therapeutic program, healthcare resources, and social services or welfare [8,9]. This review summarizes the current evidence of available neurodevelopmental assessment tools for each domain and suggests appropriate Korean surveillance guidelines for NICU graduates.

I. EARLY NEURODEVELOPMENTAL ASSESSMENT PLAN

Developmental surveillance should consider appropriate timing and intervals in terms of cost-effectiveness and availability of healthcare resources. If NICU graduates have more severe risk factors, they would be at an even higher risk of various developmental problems [10-12]. Several risk factors that must be evaluated during NICU stay are summarized in Table 1 for clinicians not to delay neurodevelopmental evaluation for referral to the Department of Pediatric Rehabilitation Medicine. According to the numbers and grades of risk factors (Table 1), a corrected age (CA) to visit for neurodevelopmental surveillance and follow-up periods are suggested in Fig. 1 [3,5,10,13,14].

Table 1.

Risk factor checklist for a surveillance of neurodevelopmental assessment after neonatal intensive care unit discharge.

Fig. 1.

Neurodevelopmental surveillance and follow-up periods according to risk factors after discharge from neonatal intensive care unit (NICU). CA, corrected age; BSID. Bayley Scales of Infant Development.

Early developmental screening is recommended within less than 1 month after discharge if there is at least one high risk factor; any organic brain lesion, such as grade 3 or 4 intraventricular hemorrhage, cystic periventricular leukomalacia, infarction, hypoxic ischemic encephalopathy, neonatal meningitis or encephalitis, and congenital brain malformation, ventriculomegaly, etc.; any feeding disorders associated with malnutrition; neonatal sepsis; bronchopulmonary dysplasia with mechanical ventilation until gestational age of 36 weeks; hyperbilirubinemia; any congenital or neuromuscular disorder, confirmed with gene study; extremely preterm (<28 weeks); extremely low birth weight (<1,000 g); high social risk such as any domestic violence or child abuse, severe poverty or homelessness, no antenatal care provided, caregivers’ intellectual disability or psychological problems; any tone abnormality of hyper/hypotonia or fluctuating tones are observed; or a history of infantile spasm or status epilepticus (Table 1). If any neurodevelopmental delay is suspected at the initial immediate follow-up, next follow-up visits or further evaluations should be determined at the physician’s discretion according to the individual infant’s medical and neurological conditions. Otherwise, later visits can be scheduled as routine follow-ups for low-risk NICU graduates. Furthermore, an immediate intervention plan and/or education can be suggested for those with high-risk factors while still in hospital, rather than waiting for a confirmative diagnosis of developmental impairments [3].

Afterwards, moderate risk factors should be screened: very preterm (28–32 weeks) or very low birth weight (1,000–1,500 g) neonates; multiple pregnancies more than twins or discordant twins who show significantly different birth weight between twins; diagnosis of sensory abnormality, such as hearing or visual impairment, and severe retinopathy of prematurity; small for gestational age, that is, birth weight less than 10th percentile for gestational age; major perinatal surgery in the brain, heart, thorax, or abdomen including necrotizing enterocolitis operation; moderate to late preterm (32–37 weeks) or low birth weight (1,500–2,500 g) with any clinical perinatal event like epilepsy or feeding problems (Table 1). If two or more moderate risk factors are present, NICU graduates are required to be followed-up for neurodevelopmental screening within less than 1 month after discharge, similar to the existence of one high-risk factor. On the other hand, if there is only 0–1 moderate risk factor, it is recommended that NICU graduates should have regular checkups at a CA of 3–4 months for the first visit. Thereafter, further follow-up visits for neurodevelopmental assessment are recommended at CA of 8–9 months, 12–18 months, 24 months, and 36 months (Fig. 1).

However, the follow-up schedule should be refined by clinicians based on the functional and/or medical status of each infant. For example, if any special diagnosis is made, such as genetic or neurodegenerative diseases, the follow-up schedule should be individualized through experts’ and multidisciplinary care plans. Although the Bayley Scales of Infant Development (BSID) is an extensive formal developmental assessment tool for diagnosing developmental delays in early childhood for 1 to 42 months old babies (Table 2), it cannot predict long-term outcomes of development, especially when assessed at a young age such as before CA of 24 months old [13,15]. For those still undiagnosed with extremely preterm birth (<28 weeks) or extremely low birth weight (<1,000 g), BSID is strongly recommended at a CA of 36 months. Likewise, individual decision-making regarding which and when each neurodevelopmental assessment tool to choose would enrich better clinical practice and more accurate assessments.

Table 2.

Summary of neurodevelopmental assessment tools in each domain; screening, motor, language-cognition, and sensory-perception function

II. OVERVIEW OF NEURODEVELOPMENTAL ASSESSMENT TOOLS

Currently available neurodevelopmental assessment tools are extremely varied at each age band. A regular neurodevelopmental follow-up program should include all developmental domains for more accurate surveillance and diagnosis, including motor, sensory perception, cognition, and language. Irrespective of how comprehensive neurodevelopmental assessment tools are employed, they are often insufficient, and clinicians should decide on additional specialized diagnostic tools for specific domains regarding individual functional status. Based on a comprehensive history taking and physical/neurological examination, including growth, primitive reflexes, postural reactions, developmental history, social/family history, and musculoskeletal evaluation, experienced clinicians should be able to decide any necessary further evaluations, including blood tests, genetic studies, or imaging modalities [5].

Categorical neurodevelopment assessment tools are summarized and compared in detail in Table 2. Each assessment tool is characterized by its target age range, test type characteristic about whether it is norm-referenced based on standard score or criterion-referenced, suggesting a clear-cut cut-off score for diagnosis, evaluation of components within domains, diagnostic criteria, average time to administer, and immediate availability of the Korean-translated version and/or education for evaluators. Among them, the Denver Development Screening Tool (DDST), BSID, Korean-Developmental Screening Test (K-DST), Peabody Developmental Motor Scales (PDMS), Korean-Wechsler Preschool and Primary Scale of Intelligence-IV, and Developmental Test of Visual-Motor Integration-6 (VMI-6) are currently covered by National Insurance in Korea.

Furthermore, currently accumulated evidence on predictive accuracy regarding the reliability, internal consistency, and validity of each development assessment tool is searched and gathered in the Supplementary Tables S1-S4 to help healthcare professionals make a more convenient decision. Reliability is the extent to which patients can be distinguished from normal despite measurement errors and is evaluated through inter-/intra-rater intraclass correlation coefficient (ICC) or Cohen’s weighted kappa values. It is “+” if ICC or kappa ≥0.70, “–” for <0.70, and “0” if no available information is found for reliability. Internal consistency is the extent to which items within a domain are inter-correlated to measure the same construct; it is “+” if factor analysis was provided with adequate sample size and Cronbach’s alpha values are ≥0.70, “–” if Cronbach’s alpha <0.70, and “0” if no available information was found for consistency. Content validity is the comprehensiveness of items in the assessment tools for the domain of interest: “+” if a clear description about the measurement aim, target population, and item selection while target population and evaluators or experts were involved in this item selection, “–” if target population or experts did not involve item selections, “0” if no information was found, and “?” if the description of these aspects is lacking. Criterion validity is the extent to which the test scores are related to a gold standard, and is demonstrated through the correlation coefficient: “+” if coefficient ≥0.70, “–” if <0.70, and “0” if no information is suggested. Construct validity is the extent to which scores on a specific domain measure the intended theoretical construct or concept. It is assessed as “+” if specific hypotheses were formulated and ≥75% of the results are in accordance, “–” if <75% of hypotheses were confirmed, “0” if no information was available, and “?” only if doubtful hypotheses or method exists [16].

Developmental delay screening

Screening tools are often used prior to an accurate diagnosis of developmental delay. A literature search for proper developmental delay screening tools, revealed that K-DST [17], and Korean-Ages and Stages Questionnaires (K-ASQ) [18,19] are available in Korean versions. The first screening is usually performed with DDST-II, inclusive of the gross motor, fine motor-adaptive, language, and personal-social domains [20]. “Delay” is indicated if a child fails an item that more than 90% of children of the same chronological age were able to do, and “caution” is indicated if a child fails an item that 75%–90% of children of the same chronological age were able to do. Developmental delay was suspected if there were two or more cautions and/or one or more delays. This criterion-based test showed a high inter-observer and test-retest reliability and sensitivity of 0.83 and specificity of 0.51, respectively [21,22]. If a developmental disorder is suspected from DDST-II, a more thorough, discriminative evaluation of BSID is usually recommended to follow as a diagnostic assessment, which is norm-based test to evaluate gross motor, fine motor, cognition, communication, social/emotional, and adaptive domains, which can suggest a high risk of developmental delay if below 2 standard deviation (<25 percentile) [23,24]. BSID is popularly used to diagnose developmental delay in terms of which domain shows a problem and how much delay is presented in terms of percentiles [18,25]. In particular, BSID at the age of 2 years is known to predict motor impairment at the age of 4 years old [10,26].

Motor function

Standardized neuromotor assessment tools are intended to discriminate or identify any abnormalities in antigravity and/or spontaneous movements elicited by infant motor patterns, reflexes, or muscle tone [27]. In contrast, most neurobehavioral assessment tools assume that the emergence of motor skills follows the same sequence as rolling, sitting, crawling, and walking and evaluate social/attentional and autonomic responses of infants according to gestational age. Although the Hammersmith Infant Neurologic Examination (HINE) evaluates both neurological and neurobehavioral domains, only a neurological domain of cranial nerve function, posture, voluntary movement, tone, and reflexes/reactions are scored to describe the risk of cerebral palsy (CP). Also, the Movement Assessment of Infants (MAI), PDMS for infant (from 2 weeks to 11 months CA), and Neurosensory Motor Developmental Assessment (NSMDA) evaluate both domains; scoring primitive reflexes, postural reactions, and muscle tone for neuromotor assessment as well as checking gross and fine motor development through observing elicited or volitional movements for neurobehavioral assessment.

The general movements (GMs), HINE, and Test of Infant Motor Performance (TIMP) are the most popular neurodevelopmental assessment tools that are recommended for the early diagnosis of CP before 5 months’ CA, together with brain imaging evaluations [14]. As well as considering risk factors (Table 1), early detection of CP or other developmental disorders can be achieved with using a combination of several standardized motor assessment tools and proper neuroimaging [14]. In infants with later infancy after 5 months’ CA, additional to HINE, the physical development domain of Developmental Assessment of Young Children, Alberta Infant Motor Scale (AIMS), and NSMDA are also recommended in combination as known to be predictive in the diagnosis of motor impairments, especially when brain magnetic resonance imaging is neither affordable nor available due to safety conditions [14,28].

During the earliest age, GM is useful and “fidgety” movement during CA between 3 and 4 months of age has been shown to have the best predictive validity of motor impairments [29,30]. Both GM and TIMP showed the strongest psychometric properties and predictive validity to better anticipate future motor outcomes and evaluate the effect of interventions [27]. On the other hand, HINE focuses more on neurologic impairment than on current motor function to propose a cutoff score in each age range to discriminate the risks of permanent motor impairment [31,32]. PDMS and AIMS have strong discriminative validity because they have a norm-referenced value from sufficiently large populations [33,34]. MAI is strong at an earlier age (younger than 4 months), such as GM and TIMP, while AIMS and NSMDA are generally for older ages (8–12-month-old) [35].

Various assessment tools exist specifically for each age band and subtest domain for NICU graduates to detect subtle changes in motor development for stratification of the severity of motor impairments and evaluation of the effect of treatment. Therefore, a uniform use of comprehensive motor assessment tools for sequential follow-up with a large population would be helpful in clarifying how NICU graduates follow and catch up on motor development milestones. Unfortunately, only PDMS is available in the formerly Korean-translated version; however, most other tools are already in common use with the English version. Although motor development is assumed to be similar in different countries, the new population displays different norms for each assessment tool [36]. Professionals involved in motor surveillance should also remember cultural effects on motor milestones and context-specific test results.

Language and cognitive function

If the language scale from the BSID results is suggestive of language function impairments, standardized language assessment batteries usually follow. New language assessment tools using the Korean language should be developed to evaluate communication skills. For comprehensive language evaluation, the Preschool Receptive-Expressive Language Scale (PRES) and the Sequenced Language Scale for Infants (SELSI) are the most popular and widely used tools with 56 questions on SELSI and 45 questions in PRES for receptive and expressive language, respectively [37]. The Paradise-Fluency Assessment (P-FA) assesses fluency using a picture representing words, sentences or speaking, and repetition task [38]; and Korean-MacArthur-Bates Communicative Development Inventories (K-M-B CDI) utilizes parent-report questionnaires about a vocabulary checklist to evaluate communication skills [39]. The Peabody Picture Vocabulary Test-Revised (PPVT-R) and the Receptive Expressive Vocabulary Test (REVT) are tools for assessing vocabulary capacity. Although different target age ranges are suggested for each assessment tool, a combination of several tools is usually recommended owing to the different test domains and scoring methods (Table 2) [37].

These language assessment tools use structured question orders, since more difficult questions for older children appear later than easier questions. Therefore, a norm-based interpretation can be used based on score distributions according to each age band, usually at 2–3-month intervals, with mean values and standard deviations. Then, the result can report the raw scores of each domain, which can be calculated as equivalent age and percentile. Picture consonant articulation test (PCAT) is only a criterion-based test that calculates percentage of correctly pronounced consonants (% accuracy). It uses an object containing the phoneme to be tested or a corresponding picture, and asks children to speak the word to evaluate the accuracy of articulation and to determine any disability or articulation based on the age at which certain consonants are acquired [40].

In Table 2, the time to administer and the availability of Korean versions/education are empty for language assessment tools. The time taken for language assessments varies considerably according to individual cooperation or cognitive level, medical status, and environment. It is difficult to accurately estimate the time required; however, 30–60 minutes are usually allocated as the evaluation time. Education for language assessment is unavailable to common users because speech and language pathologists with professional training, degrees, and national certification oversee every language assessment and treatment in Korea. Therefore, essential personnel preparation must first be established for follow-up language assessments.

As an initial screening tool for cognition, the cognitive scale from the BSID is useful for the age range of up to 42 months. The Wechsler Preschool and Primary Scale of Intelligence (WPPSI) is the most popular assessment tool for evaluating cognition. The Wechsler Intelligence Scale for Children (WISC) is for higher age, although some overlapping age bands exist around 6 to 7 years [41]. When interpreting the different results of each evaluation tool around this age, clinicians should remember that the two tests can produce a different cognitive profile, and WISC could result in lower scores on the subtest of vocabulary, matrix reasoning, and bug/symbol search compared to WPPSI [41].

Sensory-perception function

Sensory perception is important in early development, especially during critical periods of neuroplasticity and refinement [42]. Because most early interventions focus on an enriching environment for this neuroplasticity, the existence of sensory deprivation is a huge barrier for NICU graduates to catch up on developmental milestones after discharge. Most NICU graduates suffer from visual perception, visual-motor integration, and coordination impairments that affect later learning disabilities and school activities [43]. Therefore, appropriate sensory perception function assessments must be combined with regular developmental follow-up programs.

For visual sense assessment tools, the neonatal visual assessment is for the earliest age from 35 weeks to 1 year of age, which is appropriate for use during NICU stay [44]. Preverbal Visual Assessment (PreViAs), a simple questionnaire of 30 items, is for 0–24 months old babies [44,45], while the VMI-6, a nonverbal test using figure and shapes, culture-free, standardized easy tool, is for 2–90 years old including adults, which can provide a result of equivalent age for visual motor coordination function [46]. The Sensory Processing Measure-Preschool (SPM-P) is for preschool age of 2–5 years old and assesses how the child is processing sensory stimuli and how the sensory needs are reacting to different environments. The social participation measure is unique in the SPM-P and can evaluate over/under-responsiveness to sensory stimuli [47]. Sensory Profile 2 is a recently updated version of Sensory Profile 1 for infant (0–6 months), toddler (7–35 months), and child (3–14 years old). This tool requests for caregiver observations or judgment about sensory processing patterns and impact on functional performance, giving the score for each quadrant of searching, avoiding, sensitivity, and registration [48,49]. The Test of Sensory Functions in Infants (TSFI) tests five domains: tactile deep pressure, visual tactile integration, vestibular functions, ocular motor control, and reactivity to vestibular stimulation [50,51]. A stronger understanding of how children’s sensory processing patterns can impact daily function, participation, and daily activities is needed to plan further interventions.

CONCLUSION

This guideline summarizes neurodevelopmental surveillance methods for patients who have been cared for and discharged from the NICU until the age of approximately 3 years. This is based on risk factor stratification and currently available assessment tools for each development domain. This surveillance program aims to enable early diagnosis and timely intervention for people with developmental disorders to support their functions and quality of life. Although there is still a lack of evidence-based early treatment guidelines for NICU graduates, this standardized post-discharge neuromotor development surveillance program would lead to a more concrete database for identifying those who need early rehabilitation interventions in the future.

Notes

Jeong-Yi Kwon, Bo Young Hong, and Jin A Yoon are the editorial board members of Annals of Rehabilitation Medicine. The authors did not engage in any part of the review and decision-making process for this manuscript. Otherwise, no potential conflict of interest relevant to this article was reported.

Conceptualization: Kwon BS, Kwon JY. Methodology: all authors. Formal analysis: all authors. Funding acquisition: Kwon BS. Project administration: Kwon JY, Hyun SE. Visualization: all authors. Writing – original draft: Hyun SE, Kwon JY, Kwon BS, Hong BY, Yoon JA, Choi JY, Hong J. Writing – review and editing: all authors. Approval of final manuscript: all authors.

Acknowledgements

This study was supported by the Korean Society of Pediatric Rehabilitation and Developmental Medicine.

SUPPLEMENTARY MATERIALS

Supplementary materials can be found via https://doi.org/10.5535/arm.23038.

Summary of current evidence of neurodevelopmental assessment tool

Supplementary Table S1.

Current evidence of neurodevelopmental assessment tool for screening

arm-23038-Supplementary-Table-1.pdf

Supplementary Table S2.

Current evidence of neurodevelopmental assessment tool for motor function

arm-23038-Supplementary-Table-2.pdf

Supplementary Table S3.

Current evidence of neurodevelopmental assessment tool for cognitive function

arm-23038-Supplementary-Table-3.pdf

Supplementary Table S4.

Current evidence of neurodevelopmental assessment tool for sensory-perception function

arm-23038-Supplementary-Table-4.pdf

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High risk factors
Brain lesion
Grade 3 or 4 intraventricular hemorrhage
Cystic periventricular leukomalacia
Infarction
Hypoxic ischemic encephalopathy
Neonatal meningitis OR encephalitis
Congenital brain malformation, ventriculomegaly, etc.
Any feeding disorders associated with malnutrition
Neonatal sepsis
Bronchopulmonary dysplasia with mechanical ventilation until gestational age of 36 wk
Hyperbilirubinemia (bilirubin >400 μmol/L or clinical evidence of bilirubin encephalopathy)
Diagnosis of genetic or neuromuscular disease (spinal muscular atrophy, myopathy, etc.)
Extremely preterm (less than 28 wk)
Extremely low birth weight (less than 1,000 g)
High social risk (e.g., domestic violence, previous child abuse, severe poverty or homelessness, no antenatal care, intellectual disability or psychologic problem of caregiver, multicultural family)
Tone abnormality (definite hyper- or hypotonia, fluctuating tone)
History of infantile spasm or status epilepticus
Moderate risk factors
Very preterm (28–32 wk) OR very low birth weight: less than 1,500 g
Multiple pregnancy (more than twin, or twin discordance such as a significant birth weight difference in twins)
Known sensory abnormality (hearing, vision [including severe retinopathy of prematurity], etc.)
Small for gestational age: birth weight <10th percentile for gestational age
Major surgery including necrotizing enterocolitis operation (brain, cardiac, thoracic, or abdominal)
Moderate to late preterm (32–37 wk) OR low birth weight: less than 2,500 g
Any clinical event during perinatal period (seizure event, feeding problem etc.)

Table 2.

Summary of neurodevelopmental assessment tools in each domain; screening, motor, language-cognition, and sensory-perception function

Assessment tool	Age range	Test type	Components tested	Diagnostic Criteria	Time to administer (min)	Availability of Korean version & education	Equipment/cost
Developmental delay screening
DDST-II	0–6 yr	Criterion	Personal-social, fine motor-adaptive, language, gross motor	<Item interpretation>	10–30	Korean ver.: available	Manual: ₩ 10,000
				Caution: items that can be completed by 75%–90% of children but are failed		Education: none	Total equipment: ₩ 130,000
				Delay: items that can be completed by 90% of children but are failed
				<Overall interpretation>
				- Abnormal: in each area of development, more than 2 delays
				-Caution: 1 delay and/or 2 or more caution
				-Normal: no more than one caution
K-DST	4–71 mo	Norm	<18 mo: gross motor, fine motor, cognition, language, social skills	Cutoff points at each domain, age	5–10	Korean ver.: available	Free (provided by Korea Centers for Disease Control and Prevention)
		(3,010 children, Korea, 2010)	≥18 mo: same as above & self-help	-Recommendation for further evaluation: <-2 SD		Education: National Health Insurance Corporation
						Online education
				-Need for follow-up: -1 SD to -2 SD
				-Peer level: -1 SD to +1 SD
				-High level: >+1 SD
K-ASQ	4–60 mo	Criterion	Communication, fine motor, gross motor, problem solving, personal-social	-Further assessment needed: at least one score below cutoff	10	Korean ver.: available
				-Provide learning activities & monitor: at least one score adjacent to cutoff		Education: none
				-Development is on track: all scores from each domain are above cutoff		Education: none
Developmental delay diagnosis (discriminative)
BSID-III^a)	1–42 mo	Norm	Gross motor, fine motor, cognitive, communication, social/emotional, adaptive	Developmental delay:	30–90	Korean ver.: available	1 set: ₩ 1,380,000
BSID-III^a)	1–42 mo	(1,700 children from USA, 2000)		<25-percentile or below 2 SD	30–90	Education: DVD, webinars, and workshops
Motor function evaluation
GMs	Preterm–5 mo	Criterion	Visual inspection of spontaneous movement	Preterm–6 wk: writhing movement	5–20	Korean ver.: none	Free
				-Normal		Education: 4–5 day of authorized training course from GMs trust, providing certificates for each course (Basic, Advanced)
				-Abnormal (poor repertoire, cramped synchronized or chaotic)
				9–20 wk: fidgety period
				-Present
				-Abnormal
				-Absent
TIMP	34 wk	Norm	Gross motor: 42 items of postural and selective control of movement	Raw score	20–40	Korean ver.: none	25 test forms: $68
	(PMA)–4 mo	(990 infants, at risk of poor neurological outcome, USA, 2006)	- 13 Observed items for	Percentile rank (<5%, 5%–15%, 15%–25%, 25%–50%, 50%–75%, 75%–95%, >95 percentile)		Manual: $38
	(17 wk post-term)		spontaneous movement:	Age standard:		Workshops, or e-Learning Course: thetimp.com	Basic kit: $189 (including ball, cloth, rattle, etc.)
			yes-no; 1-0 scores	-Average
			- 29 Elicited items in supported sitting, supine, prone, side lying, supported standing:	-Below average: -1 SD to -2 SD
			0-3, 0-4, 0-5, 0-6 scores	-Far below average: <-2 SD
MAI	0–12 mo	Criterion	Gross motor, fine motor, muscle tone, primitive reflex, automatic reactions, volitional movements	Cutoff of total scores (not validated)	30–90	Korean ver.: none	Standardized equipment is necessary (including 2 chairs, bell, rattle, red ball, etc.)
	(m/c 4 mo)			Developmental delay or abnormal		Manual: free
				: suspect 8–13		Training recommended 2-day seminar; currently not available
				: high risk >13
			Total 65 items	: later neurological abnormality >10
			-Muscle tone: 1–6-points	: most probably normal <4
			-Others: 1–4 points
			-High risk +1 points for each item
AIMS	0–18 mo	Norm	Gross motor (no. of items)	Among all observed voluntary movements, the highest and lowest development stages are scored as window score	20–25	Korean ver.: none	50sheets : $48.95
		(2,200 infants, Canada, 1990–1992)	Prone (21), supine (9),	Previous items created (below window score) are all checked as +1	Observation for each posture (without cue): ≥5 min recommended	Guideline book: $80
			sitting (12), standing (16)	Age-adjusted subscale score (sum)
			: total 58 items	Developmental delay or abnormal:
			Items observed as voluntary movements are identified among above 4 posture-specific items	-At CA 4 mo: <10th percentile
				-At CA 8 mo: <5th percentile
HINE^b)	2–24 mo	Criterion	Scorable 5 domains:	Each item 0–3 points	10–15	Korean ver.: none	Scoring sheets (on-line free)
			-Cranial nerve function	Total score: 0–78		Guideline book
			-Posture			: $100
			-Movements	: optimal		Workshops, teaching videos (online); currently not available anymore	https://bpna.org.uk/userfiles/HINE%20proforma_07_07_17.pdf
			-Muscle tone	-At 3 mo: >67
			-Reflexes and protective reactions	-At 6 mo: >70
				: risk of cerebral palsy
			Non-scorable domains:	-At 3 mo: ≤56
			-Motor milestones	-At 12 mo: ≤65
			-Behavior	<40: severe CP risk (non-ambulatory):
				-More predictive with general movement assessment together
				- Evaluation of right-left discrepancy is possible
PDMS-II	0–6 yr	Norm	A total of 6 subsets	Raw scores for each subtest	45–60 (20–30 if only for motor-related subtest)	Korean ver.: available (for research-use only)	Kit: ~$550
	(using CA until 2 yr)	(2,003 infants, USA & Canada, 1997–1998)	A. Gross motor	Sum scores converted to standard score, %rank, age-equivalent			Test kit provides most of all equipment
			-Reflex: 2 wk–11 mo	Standard score sum		Manual: $100	Online scoring & report system: available
			-Stationary: body control	TMQ (total motor quotient)
			-Locomotion: transfer	-GMQ (gross motor quotient)
			(crawling, walking,	-FMQ (fine motor quotient)
			running, hopping, jumping)
			-Object manipulation: 12 mo~	<-1 SD : below average, caution
			: catch, throw	<-2 SD: suspicious of developmental delay
			B. Fine motor
			-Grasping: hand function
			: hold, pincer grasp, buttoning/unbuttoning, etc.
			-Visual-motor integration:
			complex eye-hand coordination
NSMDA	1 mo–6 yr	Criterion	6 Subscales (gross motor, fine motor, neurological, primitive reflexes, postural reactions, motor response to sensory input); abnormal, suspicious, normal	Functional score	20–45	Korean ver.: none	Specific toys required but easily accessible
				6–8: normal motor function		Comprehensive manual: £35
				9–11: minimal motor problem
				12–14: mild motor problem
				15–19 moderate motor problem
				20–25 severe motor problem
				>25 profound disability
Language function evaluation (Korean)
SELSI	4–35 mo	Norm	56 Questions for receptive and expressive language, respectively	Raw scores, equivalent age, percentile for semantics, phonology, syntax, and pragmatics			₩ 123,300 (including all equipment and manual)
				<-1 SD: caution
				<-2 SD: advised for further evaluation about language delay
PRES	2–6 yr (preschool)	Norm	45 Questions for receptive and expressive language, respectively	Raw scores, equivalent age, percentile for semantics, phonology/syntax, and pragmatics			₩ 300,000 (including all equipment and manual)
PRES		Norm
P-FA	Preschool, elementary & middle school	Norm	Fluency: word picture, repetition, sentence picture, reading, story picture, speaking picture (according to age level)	Raw scores, score distribution and percentile			₩ 361,000 (including all equipment and manual)
P-FA		Norm	Communication skills (not in preschool evaluation): any burden/difficulty in speaking or stuttering	Raw scores, score distribution and percentile
K-M-B CDI	8–17 mo (infant)	Norm	Parent-report form to evaluate communication skills	Level I (infant): words and gestures; short form – 89-word vocabulary checklist			₩ 90,000 (including all equipment and manual)
	18–30 mo (toddler)			Level IIA/B (toddler): words and sentences; 100-word productive vocabulary checklist, questions about combining words

PPVT-R	2 yr–8 yr 11 mo	Norm	Language comprehension,	The first question is determined by age,			₩ 1,400,000 (including all equipment and manual)
			receptive vocabulary skills	If 8 correct answers consecutively, this point is set as the baseline. (all questions before the point are scored as correct)
			: Total 178 vocabulary	If 6 out of 8 consecutive questions are incorrect, the last incorrect questions is the upper limit;
				Raw score with only correct answers to be calculated as percentile, equivalent age
REVT	2 yr 6 mo–16 yr	Norm	Receptive/expressive vocabulary skills (initially developed for Korean vocabulary)	Scoring is same with PPVT-R			₩ 380,000 (including all equipment and manual)
			: 185 Questions (using pictures) for receptive and expressive domain, respectively	<-1 SD: below average, caution
				<-2 SD: advised for further evaluation for vocabulary development

PCAT	2–12 yr or preschool	Criterion (% accuracy)	Ability to modulate consonant pronunciation (using pictures)	For speech therapy for articulation,
PCAT			: 30 Words including 43 phonemes	: consider <-1 SD, demand <-2 SD
Cognitive function evaluation
K-WPPSI-IV	2yr6mo - 3yr11mo &	Norm	FSIQ	Raw scores from the subset	30–60
	4yr - 7yr7mo		Primary index scale (comprehensive cognitive functioning): composite scores of verbal comprehension index, visual spatial index, working memory index and fluid reasoning index, processing speed index for older age band	Age-corrected standard scores of scaled and composite scores (percentile) for FSIQ and each subset scores
			Ancillary index scale: verbal acquisition index, nonverbal index, general ability index and cognitive proficiency index for older age band
Sensory-perception function evaluation
VMI-6	2–90 yr	Norm (1,882 Korean, 2–90 yr)	Visual-motor integration, visual perception, motor coordination (spontaneous scribbling task, imitated scribbling task, imitation task)	Raw scores: success until 3 consecutive fails	10–15	Korean ver.: available	With manual
				Equivalent age, standard score, percentile for screening visual motor coordination function		Education: none	: ₩ 110,000
							Without manual
							: ₩ 90,000
Neonatal Visual Assessment	GA 35 wk–1 yr	Norm (110 healthy full-term neonate at 72 h, Italy)	9 Items of spontaneous ocular motility, ocular movements with target, fixation, tracking (horizontal, vertical, arc), reaction to a colored contrast target, ability to discriminate stripes, attention at distance	Each item scored 0 if <90 percentile, scored 1 if abnormal	5–10	Korean ver.: none	Free
						Education: none
				Global score ≥2: abnormal
PreViAs	CA 0–24 mo	Norm (298 children from Spain)	Questionnaires of 30 items, 4 domains	Mean scores of each domain		Korean ver.: none	Free
PreViAs	CA 0–24 mo		: visual attention; visual communication; visual-motor coordination; visual processing	Cutoff points for each visual domain and each age group by 2 mo		Education: none	Free
SP1	Infant SP1	Norm (1,037 children without disability, 32 children with autism and 61 with ADHD from USA)	Sensory processing (auditory, visual, vestibular, touch, multisensory, oral sensory),	Sensory seeking, emotionally reactive, low endurance/tone, oral sensory sensitivity, inattention/distractibility, poor registration, sensory sensitivity, sedentary, fine motor/perceptual	20–30	Korean ver.: available	Questionnaire: $193
	0–6 mo		Modulation (sensory processing related to endurance/tone, body position/movement, movement affection activity level, sensory input affecting emotional responses, visual input affecting emotional responses and activity),	Typical performance		Comprehensive manual
	Toddler SP1		Behavioral and emotional responses (emotional/social responses, behavioral outcomes of sensory processing, items indicating thresholds for responses)	<-1 SD: possible difference		: included in questionnaire	No special equipment
	7–36 mo			<-2 SD: definite difference
	SP1 3–10 yr
	Adolescent/adult SP1 ≥11 yr
SP2	Infant SP2	Norm (1,791 from USA)	Sensory sections: auditory, visual, touch, movement, body position, oral	Seeking score: degree to which a child obtains sensory input	5–20	Korean ver.: none	Questionnaire: $292
	0–6 mo		Behavioral sections: conduct, social emotional, attentional	Avoiding score: degree to which a child is bothered by sensory input		Comprehensive manual
	Toddler SP2		Caregiver questionnaire for 5 Likert score (1–5)	Sensitivity: degree to which a child detects sensory input (notification of sensory input)		: included in questionnaire	No special equipment
	7–35 mo			Registration: degree to which a child missss sensory input
	Child SP2			Raw scores, percentile range, standardized scores
	3–14 yr 11 mo			-1 SD to +1 SD: normal
	Short SP2			<-1 SD: less than others
	3–14 yr 11 mo			<-2 SD: much less than others
	School companion SP2			>+1 SD: more than others
	3–14 yr 11 mo			>+2 SD: much more than others
SPM-P	2–5 yr	Norm (651 typically developing children from USA)	Social participation, vision, hearing, touch, total sensory system/taste and smell, body awareness, balance and motion, planning and ideas	Typical range (T-score: 40–59)	15–20	Korean ver.: none	Paper and online kit $160
				Some problems range (T-score: 60–69)		Education: none
				Definite dysfunction range (T-score: 70–80)
TSFI	4–18 mo	Norm (196 infants as typically developing, 27 infants with delayed, 27 difficult temperament infants, USA)	24 Items of 5 domains: tactile deep pressure, visual tactile integration, vestibular functions, ocular motor control, reactivity to vestibular stimulation	Item scoring for each domain,	20	Korean ver.: none	Test kit (US $199)
				Total test score: overall score of sensory processing and reactivity		Comprehensive manual	Test kit provides most equipment
				Cut-off points to diagnose sensory integrative dysfunction		: included in test kit

DDST-II, Denver Development Screening Test-II; K-DST, Korean-Developmental Screening Test; SD, standard deviation; K-ASQ, Korean-Ages and Stages Questionnaires; BSID-III, Bayley Scales of Infant Development-III (a) version IV is also available in English from 2019; same five domains but scoring is changed from dichotomous to polytomous(2,1,0) with decreased number of items to make 30% less time needed to complete the assessment); GMs, general movements; TIMP, Test of Infant Motor Performance; PMA, postmenstrual age; MAI, Movement Assessment of Infants; AIMS, Alberta Infant Motor Scale; CA, corrected age; HINE, Hammersmith Infant Neurologic Examination (b) HNNE, Hammersmith Neonatal Neurological Examination also available); CP, cerebral palsy; PDMS-II, Peabody Developmental Motor Scales-II; NSMDA, Neuro-sensory Motor Developmental Assessment; SELSI, Sequenced Language Scale for Infants; PRES, Preschool Receptive-Expressive Language Scale; P-FA, Paradise-Fluency Assessment; K-M-B CDI, Korean-MacArthur-Bates Communicative Development Inventories; PPVT-R, Peabody Picture Vocabulary Test-Revised; REVT, Receptive Expressive Vocabulary Test; PCAT, picture consonant articulation test; K-WPPSI-IV, Korean-Wechsler Preschool and Primary Scale of Intelligence-IV (version V is also available from 2019); FSIQ, full scale intelligence quotient; VMI-6, Developmental Test of Visual-Motor Integration-6; GA, gestational age; PreViAs, Preverbal Visual AssessmentSP1, Sensory Profile 1; SP2, Sensory Profile 2; SPM-P, Sensory Processing Measure-Preschool; TSFI, Test of Sensory Functions in Infants.