Early Motor Repertoire in Infants With Biliary Atresia: A Nationwide Prospective Cohort Study : Journal of Pediatric Gastroenterology and Nutrition

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Original Articles: Hepatology

Early Motor Repertoire in Infants With Biliary Atresia: A Nationwide Prospective Cohort Study

Rodijk, Lyan H.; Bos, Arend F.; Verkade, Henkjan J.; de Kleine, Ruben H.§; Hulscher, Jan B.F.; Bruggink, Janneke L.M.

Author Information
Journal of Pediatric Gastroenterology and Nutrition: April 2021 - Volume 72 - Issue 4 - p 592-596
doi: 10.1097/MPG.0000000000003021


What Is Known/What Is New

What Is Known

  • Biliary atresia affects infants within the first weeks after birth.
  • Children with biliary atresia are at risk of impairments in all neurodevelopmental domains: motor skills, cognition, and behavior.
  • Prechtl's General Movement Assessment is a noninvasive, cost-effective, and worldwide used method to identify infants who are at risk of neurodevelopmental impairments.

What Is New

  • The early motor repertoire in biliary atresia is already affected at time of diagnosis.
  • Cholestasis may induce neurological impairments in early infancy.

Biliary atresia (BA) is a severe liver disease, manifesting within the first weeks after birth. Even despite a successful Kasai portoenterostomy (KPE), liver failure is inevitable in majority of the children. This makes BA the most frequent indication for pediatric liver transplantation (1,2). Children with BA are at risk of neurodevelopmental impairments (3,4), that may already be present at 1 to 2 years of age in children with BA who survived with their native liver (5). As infancy is a time of critical brain growth, severe liver disease at this age may have the potential to interfere with the developing brain. Infants with BA are exposed to several factors potentially influencing neurodevelopmental, such as factors related to the liver disease itself with cholestasis, intracranial hemorrhage due to vitamin K deficiency, multiple hospitalizations, growth deficits, and major surgery in early childhood (5–7). Talcott et al (7) described alterations in brain biochemistry of children with BA and suggested that prolonged cholestasis before liver transplantation adversely affects neurodevelopmental outcomes. We hypothesized that these neurodevelopmental impairments in patients with BA are already present in infancy, even before KPE, whereas the neurological status of patients with BA has not been evaluated in early infancy (Table, Supplemental Digital Content, https://links.lww.com/MPG/C137).

Only a few diagnostic methods are available for assessing infants’ early neurological status (8). One of the most reliable methods, with high sensitivity and predictive value, is based on systematic observation of the early motor repertoire using Prechtl's General Movement Assessment (GMA) (8,9). The early motor repertoire consists of various endogenously generated movement patterns, of which the general movements (GMs) are the most complex, and therefore apt for diagnostics. GMA is a noninvasive, cost-effective, and worldwide used method to identify infants who are at risk of neurodevelopmental impairments (9–12).

The aim of this study was to assess whether neurological impairments in infants with BA are already present in early infancy before KPE.



In the Netherlands, health care for infants with BA and liver transplantation is centralized in the University Medical Center Groningen. From November 2015 to November 2019 all parents of an infant suspected of BA based on biochemical parameters, ultrasound and/or biopsy, hence scheduled for a KPE, were approached for inclusion in a national prospective cohort study. Video recordings were obtained before KPE. The diagnosis of BA was confirmed during laparotomy by intra-operative findings and in case of uncertainty about the diagnosis by intraoperative cholangiography. Within the inclusion period, all infants that underwent a KPE were confirmed with BA diagnosis. Exclusion criteria were diagnoses other than BA, concurring neurological disease or birth weight ≤2000 g. Written informed consent for participation in this study was obtained from all parents/caregivers. This study was approved by the medical ethics committee (METc) of the University Medical Center Groningen.

Data Collection

Data were collected from the infants’ medical files and a demographic questionnaire that the parents filled out at inclusion. These data were cross-checked with the Netherlands Study Group for Biliary Atresia Registry. The Netherlands Study Group for Biliary Atresia Registry is a prospective Dutch nationwide database in which all clinical and follow-up data of infants diagnosed with BA are collected. Data included sex, gestational age, birth weight, age at first hospital admission for evaluation of cholestasis, and disease-related complications such as intracranial hemorrhage. Around the time of video recording the GMs, we collected data on growth, particularly height, weight, and mean upper arm circumference, and results of liver panel tests in serum. We avoided taking video recordings in the 24 hours following liver biopsy or general anesthesia.

Assessment of the Early Motor Repertoire

To assess the early motor repertoire, movements of the infants were recorded on video before KPE. During these recordings, infants were in a state of active wakefulness, partly dressed, and lying in supine position. Recordings of 10 minutes were required, in which the infant was not having hiccups or crying continuously.

From birth to approximately 2 months post-term age, GMs are called writhing movements. At 46 to 49 weeks of postmenstrual age (PMA), writhing GMs gradually disappear and so-called fidgety GMs, also called fidgety movements (FMs), emerge. FMs remain evident until approximately 60 weeks of PMA when intentional movements are starting to dominate. Apart from these FMs, the early motor repertoire in this age period consists of other movement patterns which may occur concurrent with FMs, such as visual scanning, head rotations, leg lift, swipes, and wiggling-oscillating arm movements (13,14).

For infants that were 46 weeks of PMA or younger, we scored the writhing GMs, and for infants older than 49 weeks of PMA, we scored the FMs. For infants between 46 and 49 weeks of PMA, the predominant movement pattern was scored, be it writhing GMs or FMs.

For infants with a PMA of 46 weeks or younger, writhing GMs were scored using the standard form “Detailed assessment of GMs during preterm and term age” as provided by the GM Trust. First, the quality of GMs was scored as normal or abnormal (ie, poor repertoire, cramped-synchronized, or chaotic). In addition, we computed a detailed GM optimality score (GMOS, min–max 5–42 points) for each infant (15). This score consists of 4 subscores: sequence, neck and trunk, upper extremities, and lower extremities.

For infants with a PMA of 49 weeks or older, the quality of the FMs was assessed as normal, abnormal or absent. In addition, the standard form “The motor optimality score (MOS) for 3- to 5-month-old infants-revised” was used to score the MOS (min–max 5–28 points) (13).

For infants with a PMA of 46 to 49 weeks, the predominant movement pattern was scored, be it writhing GMs or FMs, including the detailed characteristics using the matching forms of the GMOS or MOS, respectively.

Interobserver reliability of GMA is considered as high, for the assessment of both GMs (k = 0.78–0.98) and FMs (k = 0.75–0.91) (11,16,17). All recordings were blinded and evaluated by 2 trained observers (L.H.R. and J.L.M.B.), according to Einspieler et al (9) A third observer, and also expert in the field of GMA (A.F.B.), was contacted in case of discrepancy.

Definition of Normal and Atypical Motor Repertoire

We defined the motor repertoire as normal or atypical based on reference groups from the literature. Regarding writhing GMs, they were scored as atypical if the overall assessment was not normal. Healthy term-born infants have normal GMs at the end of the first week postnatally, as was reported by Ploegstra et al (18) in 33 healthy term newborn infants (gestational age 39 weeks [38, 41]), birth weight (3305 g [2760–4455]). In addition, we considered normal GMs as atypical if the GMOS was low, that is, at or below the 10th centile. For GMs recorded during the post-term period the 10th centile of the GMOS is 35, as reported by Einspieler et al ((15), Table 3 in that study), and we assumed that the 51 infants with normal GMs at post-term period in that study are representative for the general population. Our cut-off for an atypical motor repertoire therefore was set at a GMOS <36. This means that the proportion of infants with normal writhing GMs but a GMOS <36 is approximately 10%.

Regarding the recordings on which FMs were predominant, we defined the motor repertoire as atypical if FMs were abnormal (from 46 weeks onwards) or were absent (from 49 weeks onwards) (13). In addition, in case of normal FMs, from 46 weeks onwards, we defined the motor repertoire as being atypical if at least 2 of the 5 classes of the MOS were scored as nonoptimal, resulting in an MOS of 25 or lower. Previously this cut-off was also applied by Berghuis et al (19). In their study, 17 out of 97 healthy infants (17.5%) were reported to have an MOS <26 (age 14 ± 1 weeks at time of video recording, gestational age 40 ± 1 weeks, birth weight 3607 ± 494) (19). To conform this study, we defined a MOS of 25 points or lower as atypical.

Statistical Analysis

For each infant, either a GMOS or MOS was obtained depending on their PMA and predominant movement pattern, be it writhing GMs or FMs. We appraised all missing data as missing at random. Inter-rater reliability was determined by calculating the intraclass correlation coefficient (ICC) based on absolute agreement, which can be interpreted as poor (≤0.50), moderate (0.50–0.75), good (0.75–0.90), and excellent agreement (≥0.90) (20). Scores were categorized as normal or atypical, using the cut-off values as described. We used Chi-square or Fisher exact analyses to test whether proportions of infants with an atypical early motor repertoire were different from those in our references, that is, 10% for the GMOS (15) and 18% for MOS (19). Throughout all analyses a P value of <0.05 was considered as statistically significant. Statistical analyses were performed by using SPSS 23.0.


Within the inclusion period 41 infants underwent a KPE and were diagnosed with BA, of whom 40 infants (98%) were included in this study before KPE (Fig. 1: flowchart of the inclusion process). In 35 of 40 participating infants, video recordings that allowed reliable assessment of the early motor repertoire (GMOS or MOS) were obtained in the week before KPE. Patient characteristics are shown in Table 1. Median gestational age was 40 weeks (36–42), with 3 infants (9%) born <37 weeks of PMA. Reasons for missing data on the motor repertoire were missing video recordings for logistic reasons (n = 5) such as short time-period between study inclusion and KPE, and/or when the infant was continuously crying infant or having hiccups.

Flowchart of the inclusion process. BA = biliary atresia, GM = General Movements.
TABLE 1 - Patient characteristics
Patient characteristics n Number Median % Min, max
Male sex 35 11 31%
Gestational age, wk 34 40 36, 42
Birth weight, g 33 3370 2015, 4285
Intracranial hemorrhage 35 0
Age at first hospital admission, days 33 48 7, 131
Highest serum level at diagnosis
 Total bilirubin, μmol/L 35 165 87, 364
 Direct bilirubin, μmol/L 35 134 72, 334
 ALT, U/L 35 180 46, 923
 Ammonia, μmol/L 25 62 32, 103
Growth at diagnosis
 Height (SD) 35 0.05 −2.90, 1.75
 Weight (SD) 33 −0.52 −2.74, 1.43
 MUAC (SD) 34 −1.80 −2.50, −0.20
BASM 35 3 9%
Age at KPE, days§ 34 56 27, 143
BASM = biliary atresia splenic malformation syndrome; KPE = Kasai portoenterostomy; MUAC = mean upper arm circumference; SD = standard deviation.Normal values:
<17 μmol/L.
<5 μmol/L.
<60 U/L.
§Age at KPE equals age at diagnosis.

Early Motor Repertoire

Table 2 provides an overview of the infants’ early motor repertoire. Inter-rater reliability for both the GMOS and the MOS was good (ICC 0.92 [0.71, 0.98] and ICC 0.86 [0.55, 0.95], respectively). At time of diagnosis (PMA 47 weeks [42–60]), 16 infants (46%) showed an atypical early motor repertoire (9/16 GMOS, 7/19 MOS). The proportion of infants with BA with an atypical early motor repertoire (46%) was significantly higher than that in the 2 reference groups (vs 10%, P < 0.001; vs 18%, P < 0.001). When stratified for the GMOS (n = 16) and MOS (n = 19), significantly more infants with BA scored atypical on the GMOS (56% vs 10%, P < 0.001) and MOS (37% vs 18%, P = 0.04) compared with the appropriate reference groups.

TABLE 2 - Early motor repertoire in infants with biliary atresia at time of diagnosis
Early motor repertoire Number median % Min, max
Total group n = 35
 Atypical early motor repertoire 16 46%
GMOS n = 16
 GMOS total score (max 42) 35 21, 42
 GMOS score <36 (atypical) 9 56%
 Poor repertoire 8 50%
 Upper extremities (max 18) 15 8, 18
 Lower extremities (max 18) 16 10, 18
 Neck and trunk (max 4) 3 2, 4
  Variable 7 44%
  Monotonous and/or broken 9 56%
MOS n = 19
 MOS total score (max 28) 26 21, 28
 MOS score <26 (atypical) 7 37%
 Global assessment: normal FMs 19 100%
 Observed movement patterns (N > A) 19 100%
 Postural patterns (N > A) 15 79%
 Age-adequate movement repertoire:
  Present 13 68%
  Reduced or absent 6 32%
 Movement character:
  Smooth and fluent 7 37%
  Abnormal, all categories 12 63%
  Abnormal, monotonous 8 42%
A = atypical; GMOS = general movement optimality score; MOS = motor optimality score; N = normal.

At time of diagnosis 9 infants (26%) were younger than PMA 46 weeks (range 42–45), and all were scored with the GMOS form for writhing GMs. Three of those 9 infants (33%) scored below the cut-off for an atypical early motor repertoire. Thirteen infants (37%) had a PMA of 49 weeks or more (range 49–60) and were therefore scored with the MOS form for FMs. Six of those 13 infants (46%) scored below the cut-off for an atypical early motor repertoire.

The other 13 infants (37%) were in the transition period between writhing GMs and FMs (PMA 46–49), of which 7 (54%) showed predominantly writhing GMs, hence were scored with the GMOS form. Six of those seven infants (86%) with predominantly writhing GMs scored in the atypical range. The other 6 infants showed predominantly FMs, hence were scored with the MOS form. One of those 6 infants (17%) with predominantly FMs scored in the atypical range. After exclusion of those infants recorded in the transition period, 9 infants (41%) showed an atypical early motor repertoire (vs 10%, P < 0.001; vs 18%, P = 0.01).

Table 3 provides information on the relation between atypical early motor repertoire and possible risk factors. We were not able to identify any clinical variables that were significantly associated with an atypical early motor repertoire in infants with BA. We also considered that diagnostic procedures and anesthesia may be a possible risk factor and confounder of the findings. The majority of infants (n = 31, 89%) had undergone a liver biopsy under general anesthesia before the video recording, of whom 4 infants had undergone 2 biopsies (n = 4, 11%). The biopsies were taken at 2 days (range 1–8) before the video recording. Neither the number of times of general anesthesia (Fisher exact test 1.67, P = 0.61) nor the number of days between anesthesia and video recordings (z statistic −0.69, P = 0.49) were significantly related to the quality of the early motor repertoire classified as normal or atypical.

TABLE 3 - Relation between atypical early motor repertoire and demographic or clinical variables
Atypical early motor repertoire
Univariable analysis N OR (95% CI) P
Patient characteristics
 Male sex 35 2.92 (0.66, 12.82) 0.16
 Birth weight, g 33 1.00 (1.00, 1.00) 0.61
 Gestational age, wk 34 1.13 (0.69, 1.84) 0.63
 Age at time of video recording (PMA in weeks) 35 0.93 (0.79, 1.10) 0.39
Medical history at diagnosis
 Age at first hospital admission, days 33 0.99 (0.97, 1.02) 0.60
 Total bilirubin, μmol/L 35 1.00 (0.99, 1.01) 0.91
 Direct bilirubin, μmol/L 35 1.00 (0.99, 1.01) 0.82
 ALAT 35 1.00 (1.00, 1.00) 0.51
 Ammonia, μmol/L 25 0.99 (0.94, 1.04) 0.67
 Height (SD) 35 1.28 (0.68, 2.44) 0.45
 Weight (SD) 33 1.24 (0.63, 2.44) 0.54
 MUAC (SD) 34 1.24 (0.51, 3.01) 0.63
MUAC = mean upper arm circumference; N = total number of patients included in analysis; OR = odds ratio; PMA = postmenstrual age; SD = standard deviation.Norm value:
<17 μmol/L.
<5 μmol/L.
<60 U/L.


Our study demonstrates that the early motor repertoire is impaired in a considerable proportion of infants with BA. At the time of diagnosis, almost half of the infants with BA showed an atypical early motor repertoire, suggesting that neurological impairment is present already in early infancy. Compared to healthy infants, approximately 2 to 3 times more infants showed an atypical motor repertoire.

To our knowledge, this study was the first to assess the early motor repertoire in young infants with BA. Previous literature reported impaired neurodevelopmental outcomes in older children with BA, regarding all domains: cognition, behavior, and motor skills (4,21). Ng et al (5) found that neurodevelopmental outcomes in infants with BA with native liver were impaired as early as 1 year of age. Our study adds to these reports that these impairments may already be present in the first weeks after birth, even before surgical salvage treatment. As previously described in literature, there are several possible explanations for neurodevelopmental impairments in children with BA (6,7). First, it may be a result of liver failure itself, with cholestasis and elevated liver enzymes. We hypothesized that the early motor repertoire in infants with BA is affected by cholestasis, and that impairments are already present in early infancy. Bilirubin is known for its detrimental effect on the developing brain, although this effect has only been proven for unconjugated bilirubin (22). We found no significant association between GMs and serum bilirubin levels, although this may be a result of the small sample size in this study. Whether cholestasis is the main culprit of neurodevelopment impairments in patients with BA remains speculative. Second, major surgery, with general anesthesia in early childhood may be related to impaired neurodevelopment (23,24). Infants with BA in our cohort already showed an impaired motor repertoire before they underwent their first surgery. This supports our hypothesis that the neurological impairments in infants with BA may be caused by factors related to cholestasis, rather than, or in addition to, perioperative factors. A third explanation related to impaired neurodevelopment is the infants’ nutritional status. Children with BA often suffer from impaired growth. Sufficient nutritional status is essential for adequate brain development (25). In our cohort, severe growth impairments were noticed, especially regarding the mean upper arm circumference. The growth percentiles, however, were not significantly correlated to the presence of an atypical early motor repertoire; therefore, leaving this explanation is also speculative. Moreover, we are not completely informed on the growth and nutritional status of the reference groups. It has been reported repeatedly that detailed scores on GMs and MOS that persist atypical over time are predictive for impaired long-term neurological outcomes (9–11,26). Whether abnormal scores of the early motor repertoire in infants with BA are predictive for long-term neurodevelopmental outcomes, similar to other clinical groups, need to be confirmed in a further follow-up study of this cohort. It would be interesting, especially in those infants who predominantly showed writhing GMs at diagnosis, to determine the change in the early motor repertoire after KPE. Another interesting topic for future research is to assess whether the quality of the early motor repertoire, either before or after KPE, is predictive for long-term neurodevelopmental outcomes. We acknowledge that our study has several limitations. At time of diagnosis, approximately one-third of infants were in the transition age between writhing movements and FMs. This may have influenced the scores as the quality of the motor repertoire may be difficult to judge in that transition period. Nevertheless, even after exclusion of the infants recorded during the transition age, >40% of infants still showed an atypical early motor repertoire. As GMs are usually not assessed in the transition age between writhing and FMs, we did not find a proper age-matched reference group of healthy peers. The infants in our cohort were, with a PMA of 47 weeks at time of diagnosis, older than the term aged infants in the cohort of Einspieler et al (15) and younger than the 3 to 4 months old infants from the reference group of Berghuis et al (19). Literature, however, shows that healthy term-born infants show normal GMs within the first week after birth (18). Therefore, the proportion of infants with BA with atypical GMs is reason for serious concern.

A further limitation is our small sample size. Because BA is a rare liver disease, it is difficult to obtain sufficient sample sizes. As a consequence, our results should be interpreted cautiously. The small sample size also limited the exploration of risk factors for an impaired motor repertoire. International collaboration and pooling of data are highly desirable to further explore risk factors. Notwithstanding, this study had a remarkable inclusion ratio, with the inclusion of almost all (40/41) newly diagnosed infants with BA from the Netherlands within the inclusion period, offering a complete overview of their early motor repertoire. The willingness of parents to participate in this study may represent parental concern about the neurodevelopment of their child.

Based on this study, we conclude that the early motor repertoire is impaired in almost half of the infants with BA. Our data indicate that neurological impairments are already present in a considerable proportion of infants with BA at time of diagnosis, that is, before infants undergo KPE, and supports our hypothesis that the disease itself adversely affects neurodevelopment. The mechanism of how BA or cholestasis affects neurodevelopment requires further study. This study warrants close monitoring of infants with BA with an atypical motor repertoire, who may be at risk of long-term neurodevelopmental impairments.


The authors would like to thank L.A. Grutters and T.M.N. Manshanden for their assistance with collecting the video recordings.


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cholestasis; general movement assessment; liver disease; neurological status

Supplemental Digital Content

Copyright © 2020 The Author(s). Published by Wolters Kluwer Health, Inc. on behalf of the European Society for Pediatric Gastroenterology, Hepatology, and Nutrition and the North American Society for Pediatric Gastroenterology, Hepatology, and Nutrition