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Neonatal neurological examination in well newborn term Ugandan infants
EHD-04158; No of Pages 11 Early Human Development xxx (2015) xxx–xxx
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Early Human Development journal homepage: www.elsevier.com/locate/earlhumdev
Neonatal neurological examination in well newborn term Ugandan infants☆,☆☆ C.F. Hagmann a,d,⁎, D. Chan b, N.J. Robertson a, D. Acolet c,1, N. Nyombi c, M. Nakakeeto c, F.M. Cowan b a
EGA UCL Institute for Women's Health, UCL, UK Department of Paediatrics, Hammersmith and Queen Charlotte's Hospitals, Imperial College, London, UK Medical Statistics Unit, London School of Hygiene and Tropical Medicine, London, UK d SBCU Mulago Hospital, Kampala, Uganda b c
a r t i c l e
i n f o
Article history: Received 2 April 2015 Received in revised form 20 June 2015 Accepted 21 August 2015 Available online xxxx Keywords: Neurological examination Low-resource setting Healthy term-born infants
a b s t r a c t Background: Newborn neurological examinations have mostly been developed in high-resource settings with cohorts comprising predominantly white Caucasian infants. No comparison has been made with different populations. Aims: To (i) establish the range of neurological findings in apparently well newborn term Ugandan infants, (ii) compare these findings to published data for equivalent term UK infants and (iii) correlate the neurological findings with perinatal characteristics and cranial ultrasound (cUS) imaging. Methods: Low-risk term Ugandan infants were recruited from the postnatal ward at Mulago Hospital, Kampala, Uganda. Neurological examination (1) and cUS were performed. The raw data and neurological optimality scores were compared to published data from UK infants (1). Gestational age, postnatal age, sex, maternal parity and HIV status, mode of delivery, birth weight and head circumference were correlated with raw scores. Results: Ugandan infants showed significantly stronger palmar grasp, better auditory and visual orientation, less irritability and less need for consoling but had poorer tone, poorer quality of spontaneous movements and more abnormal signs than UK infants. No correlation was found between raw scores and cUS findings, gestational age, sex, birth weight and head circumference. Significantly fewer Ugandan infants had optimal scores based on the UK data. Conclusion: The neurological status of low-risk hospital-born term Ugandan infants differs from that of low-risk UK infants. The study findings have implications for assessing normality in Ugandan infants and raise concerns about the use of this UK “optimality” score in other research settings. Further work is needed to understand fully the reasons for the differences. © 2015 Elsevier Ireland Ltd. All rights reserved.
1. Introduction In 1981 Dubowitz and Dubowitz established a 32-item examination for the neurological assessment of term and preterm infants [2]. In 1996 a slightly modified version of the examination was performed on 250 low-risk term-born infants 6–48 h after birth at Queen Charlotte's and Chelsea Hospital, London; half of this cohort were reviewed between 12 and 18 months of age, and no infant was found to have significant Abbreviations: cUS, cranial ultrasound; ElCS, elective caesarean section; EmCS, emergency caesarean section; GA, gestational age; MRI, magnetic resonance imaging; SVD, spontaneous vaginal delivery. ☆ Acknowledgements: We thank the staff of the postnatal wards at Mulago Hospital for all their help in undertaking this work, and also the mothers for allowing us to examine their babies. We also appreciate the work done by Dr Lilly Dubowitz in developing this neonatal examination. ☆☆ Competing interests: none. ⁎ Corresponding author at: Division of Neonatology, University Hospital of Zurich, Frauenklinikstrasse 10, 8091 Zurich, Switzerland. E-mail address: [email protected] (C.F. Hagmann). 1 Dr Dominique Acolet sadly died before this data could be published.
neurodevelopmental delay [3,4]. The examination was subsequently reviewed and updated to form the currently used 34-item proforma. A neurological optimality scoring system was devised based on the distribution of scores for each neurological item for term-born UK infants as a means of identifying neurological optimality and sub-optimality in the early perinatal period [1]. The examination is quick and simple to perform, and can be readily learnt even by non-medical individuals [1], with good inter-rater variability [5]. The examination has been used widely for clinical and research purposes. A shortened version has been successfully tested in low-resource settings [5,6]. However to date there is no standardised study that investigates the neonatal neurological status of low-risk term-born infants in low-resource settings. This is important, as infants in low resource settings are more likely to be exposed to factors that may influence their neurological status such as infections (HIV or cytomegalovirus) during pregnancy and may have a poorer level of antenatal and intrapartum care. We found that low-risk term-born infants on the postnatal ward in a public University hospital setting in Uganda had a higher incidence of cranial ultrasound (cUS) abnormalities than
http://dx.doi.org/10.1016/j.earlhumdev.2015.08.005 0378-3782/© 2015 Elsevier Ireland Ltd. All rights reserved.
Please cite this article as: Hagmann CF, et al, Neonatal neurological examination in well newborn term Ugandan infants, Early Hum Dev (2015), http://dx.doi.org/10.1016/j.earlhumdev.2015.08.005
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C.F. Hagmann et al. / Early Human Development xxx (2015) xxx–xxx
seen in the UK population [7]. We therefore hypothesised that although apparently well and with good Apgar scores, newborn Ugandan infants would differ in their neurological exam compared to UK born infants and fewer would fall within the optimal range as defined for UK born infants. Our aim in this study was to (i) establish the range of neurological findings in apparently well newborn term Ugandan infants using our UK standardised examination, (ii) compare the findings to the published data for well term-born UK infants and (iii) to correlate their neurological findings with their perinatal characteristics and cUS imaging. 2. Methods The Institutional Review Board of the Ethics Committee, Medical School, Makerere University, Kampala, Uganda approved the study; permission from the Head of the Obstetrics Department at Mulago Hospital was also obtained. 2.1. Patients Between 24th July and 31st October 2007, 115 term infants were recruited from the postnatal wards at Mulago University Hospital, Kampala, Uganda, a major public hospital serving the general population with over 33,000 deliveries a year. Maternal informed consent was obtained by the ward nurses in the mother's own language and confirmed by the study doctors. Inclusion criteria were (i) direct admission to the postnatal ward from labour ward, (ii) gestational age (GA) ≥ 36 weeks (iii) Apgar score ≥ 8 at 5 min, and (iv) ≤ 4 days postnatal age. Antenatal and perinatal clinical details were obtained from obstetric notes and the mother. Most mothers had had some hospital based antenatal care. For the purposes of this study, women in their first pregnancy were classified as primiparous and all others were multiparous. Infants were either born by spontaneous vaginal delivery (SVD) or caesarean section (CS), which could be elective (El) or emergency (Em). ElCS was mainly done because of previous CS or a known large baby; EmCS was mainly done for failure to progress, haemorrhage, evidence for foetal stress, or cord prolapse. There was no availability of assisted delivery with forceps or vacuum extraction. 2.2. Neurological examination The infants were examined using our standardised neurological protocol [1]. Nurses familiar with the local languages were available throughout the examination; the infants were seen in a postnatal ward side-room with the mother present if she wished. FC, CH, DA, NN and NM performed the neurological examinations. NN and NM were trained by FC and DA. Initially NN and NM observed FC and DA performing the examination, scoring the examination proforma. Then “hands-on” training sessions were done and lastly, video recordings were done to evaluate the performance of NM and NN. Posters with images of each neurological item were created and posted within the side-room where the examinations took place. The results were recorded on the standard proforma containing 34 neurological items categorised into 6 groups (tone, tone patterns, reflexes, movements, abnormal signs, behaviour). Each item has a maximum of 3–5 columns arranged in a horizontal row containing a picture and/or description depicting a different response. The column that best described the infant's response or behaviour was circled. Each item was then scored from the column 1, 2, 3, 4, or 5 in which it fell. If an item fell between 2 columns, it was given the appropriate half score between the columns (e.g., items scoring between 2 and 3 scored 2.5). These scores are defined as raw scores [1]. The proforma used in the UK study (1996) was slightly different in minor ways from the proforma used in this study and the raw scores for the UK infants were amended to allow comparison to the raw scores obtained from the Ugandan infants [1].
In the UK study the distribution of the raw scores was plotted for each item and the 5th and 10th centiles were used as cutoff points. An item falling above the 10th centile was given a score of 1, between the 5–10th centiles a score of 0.5, and below the 5th centile a score of 0. A maximum score of 34 could be obtained. Scores between 30.5 and 34 were found in more than 95% of the UK study infants and were considered optimal. We applied the same process to the scores from the Ugandan infants in order to assess which scores fell in the 95th centile range for Ugandan infants and we also determined how many Ugandan infants obtained a score considered optimal for the UK population. When devising the UK system, infants were excluded if their birth GA was b37 weeks, their age at examination was outside 6–48 h, their Apgar score was b 5 after 1 min and b7 after 5 min or if their cord pH level was b 7.2. When comparing the UK and Ugandan findings the same exclusion criteria were therefore applied to the Ugandan cohort apart from cord pH as this data was not available. Birth weight was taken from the clinical notes and the head circumference was measured by us, using a disposable paper tape measure. Centiles were calculated using the LMS growth calculator (www. healthforallchildren.co.uk) from WHO2006. All infants had a cUS examination (data previously published (7)). Correlations between neurological optimality scores and cUS findings were studied. 3. Results 3.1. Patients Demographic details of the cohort are given in Table 1. Of the 115 recruited and examined infants, 96 infants were born between 37 and 42 weeks GA; 9 infants under 37 weeks GA were not included in the analysis. In ten of these 96 infants the GA was recorded only as “term age”. As there were no differences in neurological raw scores between these infants and those with a documented GA, they were analysed together. There was no statistically significant difference in median Apgar scores at 5 min between infants born by SVD, EmCs and ELCS respectively. The mean GA (SD) of the included Ugandan infants with known GA was 39.1 (±1.3) compared to 39.7 (±1.2) for the UK cohort (p = 0.001). Median Apgar scores at 1 and 5 min were 8/10 and 9/10 for the Ugandan and UK cohort respectively. There was no significant difference in birth weight (3.2 vs. 3.3 kg) or head circumference (34.9 vs. 34.5 cm) between the Ugandan and UK cohort. Fifty-six of the 96 infants were examined within 6 to 48 h of birth and of those 44 had all items scored, hence, an optimality score from those 44 could be calculated and directly compared to the UK data.
3.2. Neurological examination: raw scores 3.2.1. Correlation between raw scores, age at examination, birthweight and head circumference Although the difference was not statistically significant, infants who were examined between 48 and 96 h had higher scores than those examined before 48 h. There was no correlation between raw scores and birth weight. Infants with smaller heads performed more poorly on sucking (p b 0.01) and placing (p = 0.03) than infants with larger heads and infants with smaller heads required more consoling (p b 0.01). 3.3. Correlation between raw scores and gender Female infants had a significantly stronger leg traction response (higher score, more active tone) than male infants (p b 0.01). No other item was significantly different between male and female infants.
Please cite this article as: Hagmann CF, et al, Neonatal neurological examination in well newborn term Ugandan infants, Early Hum Dev (2015), http://dx.doi.org/10.1016/j.earlhumdev.2015.08.005
C.F. Hagmann et al. / Early Human Development xxx (2015) xxx–xxx Table 1 Maternal and neonatal demographic details. TR, mother tested and results given to the mother; TRR, mother tested and result reacted (i.e. follow-up organised); TRRDm, mother tested, results reacted and mother dosed; TRRDmDb, mother tested, results reacted and mother and baby dosed. Demographic details (n = 115) Gestational age (median (range), weeks) 35–36 weeks 37–39 weeks 40–42 weeks Term age Birth weight (median (range), grammes) Number below 3rd centile according WHO 2006 Number above 97th centile according WHO 2006 Head circumference (median (range), cm) Number below 3rd centile according WHO 2006 Number above 97th centile according WHO Females (%) Mode of delivery (%) Vaginal delivery Caesarean section (CS) Emergency CS Elective CS Unknown Apgar score at 5′ (%) 10 9 8 7 Unknown Maternal parity (%) Primigravida Multiparous Age at examination (median (range), days) HIV status (%) TR TRR TRRDm TRRDbDm Unknown
38 (35.0–42.0) 8% 55% 28% 9% 3300 (1900–4800) 4 1 35.0 (31.0–37.5) 2 0 46 59 8 16 15 2 63 12 10 4 11 44 56 2 (0–4) 76 3 1.5 1.5 18
3.4. Correlation between raw scores and maternal parity Infants born to multiparous mothers had greater passive arm recoil (p = 0.02), poorer neck extensor (p b 0.01) and flexor tone (p b 0.01) and fewer abnormal hand and toe postures (p = 0.04).
3.5. Correlation between raw scores and maternal HIV status The following items were different between infants born to HIVpositive (n = 7) and HIV-negative mothers; neck flexor and extensor tone (p b 0.01), the placing reflex (p b 0.01) and quality of spontaneous movements (p = 0.04) were all poorer in infants born to HIV-positive mothers.
3.6. Correlation between raw scores and mode of delivery Infants born by EmCS had tighter popliteal angles (p b 0.049) and less startling (p = 0.03) than those born by ElCS and by SVD.
3.7. Correlation between raw scores and cUS abnormalities The cUS findings in these infants did not correlate with any raw scores [7]. Only 3 infants had findings suggestive of haemorrhage or infarction. Cysts, either in the caudothalamic notch or the choroid plexus, were seen in 19% of the infants but these infants did not differ in terms of neurological exam from infants without these findings.
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3.8. Neurological examination: optimality scores (n = 44) 3.8.1. Correlation between neurological optimality scores and gestational age There were no significant differences in optimality scores between infants born at 37–38 weeks, 39 to 40 weeks and those born at 41– 42 weeks GA (Table 2). Of the infants born between 39 and 40 weeks, 75% had optimal scores based on the UK data as did 60% of the infants born between 37 and 38 weeks; the 4 infants born after 41 weeks all had sub-optimal scores. 3.9. Comparison of neurological optimality scores between UK and Ugandan infants Forty-four infants had raw scores for each neurological item obtained between 6 and 48 h so that a total neurological optimality score could be calculated. The mean (SD) optimality score for the Ugandan infants was 29.7 (3.5) compared to 32.87 (1.7) for UK infants. Significantly fewer infants had an optimal score based on the UK data (N30.5) in the Ugandan cohort compared to the UK cohort (61% vs 95%). When the UK optimality scoring system was applied to infants who were examined between 48 and 96 h (n = 30), the mean optimality score was 31.20 (2.3) and 81% of the Ugandan infants had a score in the UK optimal range i.e. older infants had higher optimality scores but this difference did not reach significance. Fig. 1a–e show which items were significantly different between the British and Ugandan cohort. Fig. 2a–f illustrates the scored items of the UK and Ugandan infants. Tone items: UK infants had more flexed postures, greater passive arm and leg recoil, more active arm and leg traction, greater neck tone in flexion and extension, better attempts to raise the head in response to traction in the sitting position and greater limb flexion in ventral suspension compared to Ugandan infants. Ugandan infants had reduced hamstring tightness compared to UK infants. Tone pattern items: The Ugandan infants had significantly increased extensor tone item pattern compared to the UK infants. Reflexes: Tendon reflexes were more easily detected in the UK infants. The Ugandan infants had stronger palmar grasps. The UK infants had better placing and Moro reflex responses. Movements: UK infants exhibited significantly better quality of spontaneous movements and had better head raising responses to being placed in the prone position. Abnormal signs: Ugandan infants had significantly more abnormal hand and toe postures and less startling. Behaviour: Ugandan infants had more abnormal eye appearances. Auditory and visual orientations were better in the Ugandan infants. Ugandan infants were less irritable and required less consoling. A scoring system to identify neurological optimality and suboptimality was devised from the data from 94 term-born Ugandan infants examined within 96 h birth (Table 3). The median postnatal age of the infants at examination was 2 days. The range of total neurological scores was 27–34. Scores between 29 and 34 were found in more than 95% of the Ugandan infants and, therefore scores equal to and above 29 can be considered optimal. 4. Discussion It has been shown that neurological examination [8,9] within 6 h of birth can serve as a clinical biomarker for patient selection in cooling trials [10]. Shankaran et al reported that early neurological examination may serve as a marker for brain injury after hypoxia ischaemia as well as a response to treatment [11]. Detailed neurological examination in term infants with neonatal encephalopathy using the Hammersmith neonatal examination after the second postnatal week was predictive of neurodevelopmental outcome [12]. The lowest scores were associated with severe basal ganglia and white matter injury as seen on
Please cite this article as: Hagmann CF, et al, Neonatal neurological examination in well newborn term Ugandan infants, Early Hum Dev (2015), http://dx.doi.org/10.1016/j.earlhumdev.2015.08.005
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Table 2 Application of the UK term-born total neurological optimality scoring system to term-born Ugandan infants. Gestational age at birth
Optimality scores, mean (SD) No. (%) of infants with optimal scores No. (%) of infants with suboptimal scores
37–38 weeks (n = 20)
39–40 weeks (n = 20)
41–42 weeks (n = 4)
Total (n = 44)
29.5 (4.1) 12 (60) 8 (40)
30.25 (3.3) 15 (75) 5 (25)
28.25 (1.2) 0 (0) 4 (100)
29.73 (3.6) 27 (61) 17 (39)
magnetic resonance imaging (MRI), hence, optimality scores gave prognostic information on the severity of functional motor outcome in this population [13]. A study combining serial detailed neurological examination with brain MRI findings showed that the evolution of neurological findings (examined within 1–2 weeks, 5–7 weeks and at 6 months) is different in infants with different MR brain lesions [14]. We found a significant correlation between cUS abnormalities and neurological findings in cooled and non-cooled Ugandan infants
with perinatal asphyxial encephalopathy (unpublished data). This highlights the importance of neurological examination in clinical and in research settings. However, as we show in this study, validated optimal normative data from one population might not be applicable to another population with a different cultural background. This study presents significant differences in neurological items between the UK and the Ugandan infants. Ugandan term infants had poorer tone, poorer quality of spontaneous
Fig. 1. A. Ventral suspension. When held in ventral suspension, this infant's head was almost in line with the body and the limbs were flexed. This infant scored 3. B. Moro reflex. This infant's shoulders were abducted but there is was adduction of the arms. This infant scored 2. C. Head raising prone. Whilst in the prone position, this infant was able to lift their head but was unable to raise their chin off the bed. This infant scored 2. D. Abnormal hand or toe postures. This infant had continuous fisting and scored 4. E. Visual orientation. This infant had normal visual responses. The head turned towards the target. This infant scored 4.
Please cite this article as: Hagmann CF, et al, Neonatal neurological examination in well newborn term Ugandan infants, Early Hum Dev (2015), http://dx.doi.org/10.1016/j.earlhumdev.2015.08.005
C.F. Hagmann et al. / Early Human Development xxx (2015) xxx–xxx
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A) Tone and posture column 1
column 2
column 3
Legs slightly flexed
Leg well-flexed but not adducted
Posture
Arms & legs extended
Arm traction
Arm recoil
Arms do not flex
Arms remain straight; no resistance
↑
Head control 2
Head control 1
Popliteal angle
Leg traction
Leg recoil
No flexion
Legs straight - no resistance
↑
Arms flex slowly; not always; not completely
Arms flex slightly or some resistance felt
↑
Incomplete flexion; not every time
Legs flex slightly or some resistance felt ↑
Arms flex slowly; more complete
Arms flex well till shoulder lifts, then straighten
column 4 Leg well flexed & adducted near abdomen
Arms flex quickly and completely
column 5
Arms difficult to extend; snap back forcefully
↑
Flexion of arms <100°; mantained when body lifts up ↑
Complete but slow flexion
Complete fast flexion
Legs difficult to extend; snap back forcefully
↑
Knee flexes -well; remains flexed when bottom up ↑
1
b)
Arms flex well approx 100° & mantained as shoulder lifts ↑
Legs flex well till bottom lifts up
1 .5 2 .5 3 .5 4 .5 5
Abnormal posture: a) opistotonus
Flexion stays when back+bottom up ↑
No attempt to raise head
No attempt to raise head
Infant tries: effort better felt than seen
Infant tries: effort better felt than seen
≈ 110°
Raises head but drops forward or back
Raises head but drops forward or back
≈90°
2
1
40
1
56
Ugandan
6
<1
23
4
66
UK
46
5
39
22
9
67
UK
43
2
53
Ugandan
8
3
87
UK
35
4
44
2
6
Ugandan
15
11
69
1
2
UK
79
1
2 1
<1
8 <1
1
15
Tries to lift head but it drops back
Able to lift head slightly
Lifts head in line with body
Back curved, head ↓, limbs slightly flexed
Back slightly curved, limbs flexed
Back straight, head in line, limbs flexed
1
Ugandan
Ugandan
3
4
24
13
56
UK
1
10
1
36
2
49
Ugandan
1
4
30
17
48
UK
Head upright or extended; cannot be passively flexed
1
41
1
50
Ugandan
31
19
47
UK
61
1
9
Ugandan
6
41
14
28
UK
18
2
46
2
29
5
4
56
14
22
7
Head in front of body
5
23 12
Back curved, head & limbs hang straight
1
1
<90°
Head lag Ventral susp.
83
<1
<1
UK
5
4
Head drops & stays back
Ugandan
8
1
Raises head: remains vertical it may wobble
Raises head: remains vertical it may wobble
19
<1
7
<1
≈ 150°
4
1
5
180°
76
Back straight, head above body
1
2
Ugandan UK
Fig. 2. Distribution of raw scores in low-risk term-born Ugandan and UK infants. Each item on the proforma is illustrated by a strip as it is on the standard proforma and to the right of the strip are the percentages of Ugandan and UK infants, who score each raw score. The shading highlights the raw scores that were found in at least 10% of each subgroup. The cell with the highlighted border indicates the median score. All percentages are rounded to the nearest whole number. A. Tone and posture. B. Tone patterns. C. Reflexes. D. Movements. E. Behaviour.
Please cite this article as: Hagmann CF, et al, Neonatal neurological examination in well newborn term Ugandan infants, Early Hum Dev (2015), http://dx.doi.org/10.1016/j.earlhumdev.2015.08.005
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C.F. Hagmann et al. / Early Human Development xxx (2015) xxx–xxx
Flexor tone 1
B) Tone patterns On arm and leg traction
column 2
column 3
Arm flexion < leg flexion
Arm flexion = leg flexion
In supine
Inc. ext. tone
Neck ext. tone
Leg ext. tone
Flexor tone 2
Arms and legs generally flexed
Leg traction vs Leg traction > pop. angle than popliteal angle
Leg traction = popliteal angle
Neck in ext. vs neck in flexion
Head extension = head flexion
Vent susp vs head lag
Head extension < head flexion
Ventral suspension < head lag
Ventral suspension = head lag
column 4
column 5
Arm flexion> leg flexion but difference 1 column or <
Arm flexion > leg flexion and difference > than 1 column
Strong arm flexion with strong leg extension intermittent
Strong arm flexion with strong leg extension continuous
Leg traction < popliteal angle but difference 1 column <
Leg traction < popliteal angle and difference > than 1 column
Head extension >head flexion. but difference 1 column <
Head extension >head flexion and difference > than 1 column
Ventr suspension > head lag but difference 1 column <
Ventr suspension> head lag and difference > than 1 column
1 .5 2 .5 3 .5 4 .5 5 27
64
8
Ugandan
23
62
15
UK
Ugandan
100
99
UK
1
9
54
3
32
1
Ugandan
4
56
2
36
1
UK
8
85
6
Ugandan
5
91
5
UK
10
52
32
5
Ugandan
25
53
21
1
UK
Fig. 2 (continued).
movements, more abnormal signs including abnormal hand and toe postures compared to UK born infants. However, they showed stronger palmar grasp, better auditory and visual orientation, were less irritable and required less consoling than the UK infants. The Ugandan infants had detailed cUS and there was no correlation between cUS abnormalities and neurological findings but only very few infants had any imaging findings of definite concern (3%) [7]. Furthermore, they all had 5 minute Apgar scores in the normal range, which were not different from our UK cohort and they did not have signs of neonatal encephalopathy or other clinical problems to explain the supposed sub-optimal neurological findings. Therefore, one can speculate, that the neurological findings, which seems abnormal when compared to a UK population, may represent normal neurological findings in the Ugandan population. The Ugandan cohort was slightly younger than the UK cohort. Earlier birth gestation has been described in African populations. However we did not find a difference in neurological findings between those born at 37–38 weeks GA and those born later so the slightly earlier gestation is unlikely to be the explanation for the neurological differences we found, particularly given the good visual and auditory attention. We had found that that many infants had mild white matter echogenicity and/or sub-ependymal type cysts in the caudothalamic notch or choroid plexus cysts, the aetiology of
which was unclear. However these findings did not seem to relate to maternal HIV status [7] and these infants were not different neurologically from those without cysts. We had no evidence for maternal illness from the history we could obtain nor maternal drug intake or local herbal preparations. Hence we devised an optimality and sub-optimality scoring system for the Ugandan infants with scores of N 29 being defined as being optimal. To help validate whether these scores truly represent optimal neurological behaviour in this population development follow-up at 18–24 months should be done; however, this was not be feasible for us to do in this setting but is currently being done in another study of control Ugandan infants. Previous studies which compared the neurological examination between a UK, a Thai and Karen refugee camp cohort found that the Karen cohort had an overall decrease in tone and poorer vision performance than the British cohort [5]. They hypothesised that these differences might be associated with specific maternal nutritional deficiencies such as transketolase deficiency, which is common in that population. In a subsequent study with Vietnamese infants less marked differences in neurological items were found between the UK and the Vietnamese cohort and no correlation was found with transketolase levels [6]. Similar to the Asian infants, Ugandan infants had poorer tone compared to the UK infants, however their
Please cite this article as: Hagmann CF, et al, Neonatal neurological examination in well newborn term Ugandan infants, Early Hum Dev (2015), http://dx.doi.org/10.1016/j.earlhumdev.2015.08.005
C.F. Hagmann et al. / Early Human Development xxx (2015) xxx–xxx
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C) Reflexes column 1
column 2 Felt, not seen
column 3 Seen
column 4
column 5
Exaggerated
Suck/Gag
20 1
No gag / no suck
Palmar grasp
No response
Plantar grasp
No response
Moro reflex
No response or opening of hands only
Weak irregular suck only
Weak regular suck
No response
Strong suck: • irregular • regular
No suck but strong clenching
No stripping
Some stripping
Good stripping
Short, weak flexion of fingers
Strong flexion of fingers
Strong finger flexion, shoulder ↑
Partial plantar flexion of toes
Full abduction at shoulder and extension of the arms; no adduction
Dorsiflexion of ankle only
1
Very strong grasp; infant can be lifted off couch
Toes curve around the examiner’s finger
Full abduction but only delayed or partial adduction
→
Placing
1 .5 2 .5 3 .5 4 .5 5
Clonus
Tendon
Absent
2
21
76
1
5
3
2
1
1
1
3
Ugandan
<1
1
UK
91
5
Ugandan
93
2
UK
2
Ugandan
2
34
2
51
4
1
85
1
8
2
-No abduction or adduction; -Only forward extension of arms from the shoulders -Marked adduction only
3
8
6
Partial abduction at shoulder and arm extension followed by smooth adduction
71
UK
Ugandan
94 <1
97
<1
UK
8
38
4
48
1
Ugandan
1
17
3
71
8
UK
→
Full placing response with flexion of hip, knee & placing sole on surface
1 1
16 19
5
78
Ugandan
80
UK
Fig. 2 (continued).
visual and auditory orientation was better than that of the UK infants. In this study, we had no information about the maternal nutritional state. However, only three infants were small for GA, all others having age appropriate birth weight and head circumference. In the term-born UK cohort, maturation in limb and axial tone, posture and the Moro reflex was seen with increasing GA, but not in the Ugandan cohort. A reason for the lack of significant differences in the distribution of raw scores in infants born at different term GA could be the narrow range of GAs with most infants (n = 80) born between 37 and 39 weeks. Another reason could be the potential inaccuracy in determining GA of the Ugandan infants from the date of the first day of the mother's last menstrual period (LMP).
Neck flexor and extensor tone, the placing reflex and the quality of spontaneous movements were significantly poorer in Ugandan infants born to the relatively few HIV-positive mothers compared to those born to HIV-negative mothers. As the HIV status of the infants themselves was unknown, it remains speculative as to whether HIV infection had an influence on the neurological examination in these infants. However, in another study infants born to HIV positive mothers had inferior orienting scores and a greater number of abnormal reflexes on the Brazelton scale even in HIV exposed infants who do not become HIV positive [15]. HIV-infected Ugandan infants have been reported to have more motor and neurological abnormalities between 6 and 24 months of age [16]. We suggest that our neurological assessment would provide a practical tool for assessing the effects of active
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D) Movements
Movement (Quality)
Movement (Quantity)
column 1
column 2
column 3
column 4
column 5
No movement Sporadic and short isolated movements
Frequent isolated movements
Frequent generalised movements
Continuous exaggerated movements
Only stretches.
Frequent stretches and abrupt movements; some smooth movements
Fluent movements but monotonous
Fluent alternating movements of arms + legs; good variability
Cramped synchronised; mouthing jerky or other abn.mov.
Infant rolls head over, chin not raised
Infant rolls head over , raises chin
Infant brings head and chin up
Infant brings head up and keeps it up
Head raising prone
No response
1 .5 2 .5 3 .5 4 .5 5 15
81
Ugandan
4
<1
27
68
UK
7
1
73
4
<1
27
4
1
16
1
Ugandan
68
UK
42
51
2
5
Ugandan
10
50
3
37
UK
E) Abnormal signs
Startle
Tremor
Abn. hand or toe posture
column 1
No startle, even to sudden noise
column 2
column 3
column 4
column 5
Continuous fisting or thumb adduction; index finger flexion, thumb opposition
Continuous big toe extension or flexion of all toes
Hands open, toes straight most of the time
Intermittent fisting or thumb adduction
No tremor or tremor only when crying
Tremor only after Frequent Moro or tremors when occasionally awake when awake
Continuous tremors
No spontaneous startle but reacts to sudden noise
2-3 spontaneous startles
Continuous startles
More than 3 spontaneous startles
1 .5 2 .5 3 .5 4 .5 5
18
1
36
1
62
1
Ugandan
85
1
12
1
UK
89
1
7
2
Ugandan
1
UK
1
87
12
80
1
Ugandan
98
2
UK
Fig. 2 (continued).
interventions in pregnancy such as antiviral medication and antimalarials or of maternal diseases. Our observations may reflect a normal variation in the population we studied or may reflect consequences related to the minor cUS findings or the slightly earlier gestation birth or perhaps exposure to a more difficult intrauterine environment in this sub-Saharan population; it is not unreasonable to suggest that our Ugandan population may represent populations in much of Africa. The findings provide baseline data for comparison with neurological examination from sick infants from similar communities at risk of impaired neurodevelopmental outcomes such as preterm infants and/or term infants with neonatal encephalopathy or seizures. The data are also important for studies or trials of neonatal treatments in which neurological examination will be used to select for neuroprotective studies, to assess progress of disease and predict outcome.
Conflict of interest statement There is no conflict of interest.
Funding This project was initiated as part of the Uganda Women's Health Initiative (UWHI) involving the University College London, Institute for Women's Health, Mulago Hospital, Makerere University and Hospice Africa Uganda. We are grateful to Professor Ian Jacobs and Dr Anthony Gakwaya co-directors of UWHI and Mr Graham Evans project manager of UWHI for their support and guidance. The UWHI and this project were supported by generous donations from Lee and Roger Myers and Ann-Margaret and John Walton.
Please cite this article as: Hagmann CF, et al, Neonatal neurological examination in well newborn term Ugandan infants, Early Hum Dev (2015), http://dx.doi.org/10.1016/j.earlhumdev.2015.08.005
C.F. Hagmann et al. / Early Human Development xxx (2015) xxx–xxx
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F) Behaviour Eye movements
column 1
column 2
Does not open eyes
Full conjugated eye movements
Visuaal orientation Alertness Irritability
column 4
column 5
Transient -nystagmus -strabismus -roving eye mov. -sunset sign
Persistent -nystagmus -strabismus -roving eye mov. -downward deviation
Auditory startle; brightens and stills; no true orientation
Shifting of eyes, head might turn towards source
Prolonged head turn to stimulus; search with eyes; smooth
Turns head and eyes towards noise every time; jerky abrupt
Does not follow or focus on stimuli
Stills, focuses, follows briefly to the side but loses stimuli
Follows horizontally and vertically; no head turn
Follows horizontally and vertically; turns head
Follows in a circle
Will not respond to stimuli
When awake, looks only briefly
When awake, looks at stimuli but loses them
Keeps interest in Does not tire stimuli (hyper-reactive)
Quiet all the time, not irritable to any stimuli
Awakes, cries Cries often sometimes when when handled handled
Cries always when handled
Asleep; awake, no crying; consoling not needed
Awake; cries briefly; consoling not needed
Awake; cries; becomes quiet when talked to
Awake; cries ; needs picking up to console
No cry at all
Whimpering cry only
Cries to stimuli but normal pitch
Auditory orientation
No reaction
1 .5 2 .5 3 .5 4 .5 5 1
96
3
Ugand an
8
92
<1
UK
1
1
10
1
51
4
33
Ugandan
24
6
50
5
15
UK
2 8
Cries even when not handled
Awake; cries cannot be consoled
High pitched cry; often continuous
17 2
14 12
Cry
Consolability
column 3
3
79
6
60
5
50
7
27
2
1
21
Ugandan
3
UK
37
4
47
38
1
47
38
2
44
2
UK
4
1
Ugandan
12 1
59
Ugandan
26
2
5
UK
28
4
12
Ugandan
52
2
12
UK
1
99
Ugandan
5
95
UK
Fig. 2 (continued).
Table 3 Compound optimality scores for the Ugandan total neurological optimality scoring system.
Tone and posture Tone patterns Reflexes Movements Abnormal signs Behaviour
Range of compound scores
Range of optimal compound optimality scores
Suboptimal compound optimality scores
6–10 3–5 3.5–6 1–3 1–3 4.5–7
8–10 4.5–5 5–6 2.5–3 2.5–3 6–7
b8 b4.5 b5 b2.5 b2.5 b6
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C.F. Hagmann et al. / Early Human Development xxx (2015) xxx–xxx
Appendix A Differences between the 1996 proforma on which the neurological examination results of the UK infants were recorded and the 2007 proforma on which the neurological examination results of the Ugandan results were recorded. Raw scores for the UK data were amended as shown below to match the 2007 proforma. A.1. Leg extensor tone Amendments to UK raw data: raw scores of 2 and 4 were switched.
1996
Leg traction vs pop. angle
2007
Leg traction vs pop. angle
Column 2
Column 3
Column 4
Column 5
Leg traction b popliteal angle but difference 1 column b Leg traction N than popliteal angle
Leg traction = popliteal angle
Leg traction N than popliteal angle
Leg traction = popliteal angle
Leg traction b popliteal angle but difference 1 column b
Leg traction b popliteal angle and difference N than 1 column Leg traction b popliteal angle and difference N than 1 column
A.2. Suck/gag Amendments to UK raw data: raw scores of 2 were re-scored to 3 or remained as 2, raw scores of 3 became 4, and raw scores of 4 became 5. 1996
2007
Column 1
Column 2
Column 3
Column 4
No gag/no suck
Weak suck only: ● Irregular ●Regular No stripping Weak irregular suck only No stripping
Strong suck: ● Irregular ● Regular Good stripping Weak regular suck Some stripping
No suck but strong clenching
No gag/no suck
No suck but strong clenching
Strong suck: ● Irregular ● Regular Good stripping
A.3. Spontaneous movements Amendments to UK raw data: raw scores for spontaneous movement became the raw scores for movement (quantity) and movement (quality).
1996
Column 1
Column 2
Column 3
Column 4
Column 5
No movement
Few stretches, no other movement, smooth movement
Smooth movement some jerky movement + stretches
Smooth alternating movements of arms + legs
Fits, or other abnormal movements, describe
Frequent isolated movements
Frequent generalised movements
Continuous exaggerated movements
Fluent movements but monotonous
Fluent alternating movements of arms + legs; good variability
Cramped synchronised; mouthing jerky or other abn.mov.
Spontaneous movement (quantity) 2007 No movement Sporadic and short isolated movements Spontaneous movement (quality) 2007 Only stretches. Frequent stretches and abrupt movements; some smooth movements
A.4. Abnormal hand or toe postures Amendments to UK raw data: raw scores of 1 became 2, raw scores of 2 became 3, raw scores of 3 became 4, and raw scores of 4 became 5.
1996
Column 1
Column 2
Column 3
Column 4
Hands open
Hands fist or thumbs adduct but opens Hands open, toes straight most of the time
Hands fist or thumb adducts, finger & thumb oppose always Intermittent fisting or thumb adduction
Big toe up (extends) or all toes flex always
2007
Column 5
Continuous fisting or thumb adduction; index finger flexion, thumb opposition
Continuous big toe extension or flexion of all toes
A.5. Tremor Amendments to UK raw scores: raw scores of 1 became 2, raw scores of 4 became 3, and raw scores of 4.5 became 5. Column 2
Column 3
Column 4
Column 5
1996 No tremor Tremor only when crying Tremor only after Moro Some tremor when awake Lots of tremor when awake 2007 No tremor or tremor only when crying Tremor only after Moro or occasionally when awake Frequent tremors when awake Continuous tremors
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C.F. Hagmann et al. / Early Human Development xxx (2015) xxx–xxx
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A.6. Eye movements Amendments to UK raw scores: raw scores of 2 became 3, and raw scores of 3 became 4 or 5.
1996 2007
Column 1
Column 2
Column 3
Does not open eyes Does not open eyes
Normal eye movement, eyes move together
Abnormal eye movements, describe Full conjugated eye movements
Column 4
Column 5
Transient –Nystagmus –Strabismus –Roving eye mov.
Persistent –Sunset sign –Nystagmus –Strabismus –Roving eye mov. –Downward deviation
A.7. Irritability Peak of excitement and irritability were incorporated into one item, irritability. Amendments to UK raw scores: an average of the raw scores for peak of excitement and irritability were used as the raw score for the revised irritability item. Peak of excitement (Circle ‘H’ if high pitch cry). Column 1
Column 2
Column 3
Column 4
Column 5
Quiet all the time H
Awakes briefly, does not cry H
Awakes briefly, cries sometimes H
Cries always when handled H
Cries always H
Irritability 1996 Not irritable to stimuli
Cries 1–2 times
Cries 3–4 times
Cries to all stimuli
Cries even when not handled
Irritability 2007 Quiet all the time, not irritable to any stimuli
Awakes, cries sometimes when handled
Cries often when handled
Cries always when handled
Cries even when not handled
1996
A.8. Cry This item was not present in the 1997 proforma. Amendments to UK raw scores: Infants with a raw score of 1 for Peak of excitement and Irritability on the 1997 proformas, retained their raw score of 1. Infants whose cry was recorded as high-pitched on the Peak of excitement item were given a raw score of 5. The remaining infants were given a new raw score of 3.
2007
Column 1
Column 2
Column 3
No cry at all
Whimpering cry only
Cries to stimuli but normal pitch
References [1] Dubowitz L, Mercuri E, Dubowitz V. An optimality score for the neurologic examination of the term newborn. J Pediatr 1998;133(3):406–16. [2] Dubowitz LM, Dubowitz V, Palmer P, Verghote M. A new approach to the neurological assessment of the preterm and full-term newborn infant. Brain Dev 1980;2(1): 3–14. [3] Haataja L, Mercuri E, Cowan F, Dubowitz L. Cranial ultrasound abnormalities in full term infants in a postnatal ward: outcome at 12 and 18 months. Arch Dis Child Fetal Neonatal Ed 2000;82(2):F128–33. [4] Haataja L, Mercuri E, Regev R, Cowan F, Rutherford M, Dubowitz V, et al. Optimality score for the neurologic examination of the infant at 12 and 18 months of age. J Pediatr 1999;135(2 Pt 1):153–61. [5] McGready R, Simpson J, Panyavudhikrai S, Loo S, Mercuri E, Haataja L, et al. Neonatal neurological testing in resource-poor settings. Ann Trop Paediatr 2000;20(4): 323–36. [6] Hieu NT, Gainsborough M, Simpson JA, Thuy NT, Hang NN, Taylor AM, et al. Neurological status of low-risk Vietnamese newborns: a comparison with a British newborn cohort. J Health Popul Nutr 2006;24(1):57–63. [7] Hagmann CF, Robertson NJ, Acolet D, Chan D, Onda S, Nyombi N, et al. Cranial ultrasound findings in well newborn Ugandan infants. Arch Dis Child Fetal Neonatal Ed 2010;95(5):F338–44. [8] Sarnat HB, Sarnat MS. Neonatal encephalopathy following fetal distress. A clinical and electroencephalographic study. Arch Neurol 1976;33(10):696–705.
Column 4
Column 5 High pitched cry; often continuous
[9] Thompson CM, Puterman AS, Linley LL, Hann FM, van der Elst CW, Molteno CD, et al. The value of a scoring system for hypoxic ischaemic encephalopathy in predicting neurodevelopmental outcome. Acta Paediatr 1997;86(7):757–61. [10] Gunn AJ, Wyatt JS, Whitelaw A, Barks J, Azzopardi D, Ballard R, et al. Therapeutic hypothermia changes the prognostic value of clinical evaluation of neonatal encephalopathy. J Pediatr 2008;152(1):55–8 [8 e1]. [11] Shankaran S, Laptook AR, Tyson JE, Ehrenkranz RA, Bann CM, Das A, et al. Evolution of encephalopathy during whole body hypothermia for neonatal hypoxic-ischemic encephalopathy. J Pediatr 2012;160(4):567–72 [e3]. [12] Mercuri E, Guzzetta A, Haataja L, Cowan F, Rutherford M, Counsell S, et al. Neonatal neurological examination in infants with hypoxic ischaemic encephalopathy: correlation with MRI findings. Neuropediatrics 1999;30(2):83–9. [13] Haataja L, Mercuri E, Guzzetta A, Rutherford M, Counsell S, Flavia Frisone M, et al. Neurologic examination in infants with hypoxic-ischemic encephalopathy at age 9 to 14 months: use of optimality scores and correlation with magnetic resonance imaging findings. J Pediatr 2001;138(3):332–7. [14] Ricci D, Guzzetta A, Cowan F, Haataja L, Rutherford M, Dubowitz L, et al. Sequential neurological examinations in infants with neonatal encephalopathy and low Apgar scores: relationship with brain MRI. Neuropediatrics 2006;37(3):148–53. [15] Scafidi F, Field T. Brief report: HIV-exposed newborns show inferior orienting and abnormal reflexes on the Brazelton Scale. J Pediatr Psychol 1997;22(1):105–12. [16] Drotar D, Olness K, Wiznitzer M, Guay L, Marum L, Svilar G, et al. Neurodevelopmental outcomes of Ugandan infants with human immunodeficiency virus type 1 infection. Pediatrics 1997;100(1):E5.
Please cite this article as: Hagmann CF, et al, Neonatal neurological examination in well newborn term Ugandan infants, Early Hum Dev (2015), http://dx.doi.org/10.1016/j.earlhumdev.2015.08.005
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Neonatal neurological examination in well newborn term Ugandan infants☆,☆☆ C.F. Hagmann a,d,⁎, D. Chan b, N.J. Robertson a, D. Acolet c,1, N. Nyombi c, M. Nakakeeto c, F.M. Cowan b a
EGA UCL Institute for Women's Health, UCL, UK Department of Paediatrics, Hammersmith and Queen Charlotte's Hospitals, Imperial College, London, UK Medical Statistics Unit, London School of Hygiene and Tropical Medicine, London, UK d SBCU Mulago Hospital, Kampala, Uganda b c
a r t i c l e
i n f o
Article history: Received 2 April 2015 Received in revised form 20 June 2015 Accepted 21 August 2015 Available online xxxx Keywords: Neurological examination Low-resource setting Healthy term-born infants
a b s t r a c t Background: Newborn neurological examinations have mostly been developed in high-resource settings with cohorts comprising predominantly white Caucasian infants. No comparison has been made with different populations. Aims: To (i) establish the range of neurological findings in apparently well newborn term Ugandan infants, (ii) compare these findings to published data for equivalent term UK infants and (iii) correlate the neurological findings with perinatal characteristics and cranial ultrasound (cUS) imaging. Methods: Low-risk term Ugandan infants were recruited from the postnatal ward at Mulago Hospital, Kampala, Uganda. Neurological examination (1) and cUS were performed. The raw data and neurological optimality scores were compared to published data from UK infants (1). Gestational age, postnatal age, sex, maternal parity and HIV status, mode of delivery, birth weight and head circumference were correlated with raw scores. Results: Ugandan infants showed significantly stronger palmar grasp, better auditory and visual orientation, less irritability and less need for consoling but had poorer tone, poorer quality of spontaneous movements and more abnormal signs than UK infants. No correlation was found between raw scores and cUS findings, gestational age, sex, birth weight and head circumference. Significantly fewer Ugandan infants had optimal scores based on the UK data. Conclusion: The neurological status of low-risk hospital-born term Ugandan infants differs from that of low-risk UK infants. The study findings have implications for assessing normality in Ugandan infants and raise concerns about the use of this UK “optimality” score in other research settings. Further work is needed to understand fully the reasons for the differences. © 2015 Elsevier Ireland Ltd. All rights reserved.
1. Introduction In 1981 Dubowitz and Dubowitz established a 32-item examination for the neurological assessment of term and preterm infants [2]. In 1996 a slightly modified version of the examination was performed on 250 low-risk term-born infants 6–48 h after birth at Queen Charlotte's and Chelsea Hospital, London; half of this cohort were reviewed between 12 and 18 months of age, and no infant was found to have significant Abbreviations: cUS, cranial ultrasound; ElCS, elective caesarean section; EmCS, emergency caesarean section; GA, gestational age; MRI, magnetic resonance imaging; SVD, spontaneous vaginal delivery. ☆ Acknowledgements: We thank the staff of the postnatal wards at Mulago Hospital for all their help in undertaking this work, and also the mothers for allowing us to examine their babies. We also appreciate the work done by Dr Lilly Dubowitz in developing this neonatal examination. ☆☆ Competing interests: none. ⁎ Corresponding author at: Division of Neonatology, University Hospital of Zurich, Frauenklinikstrasse 10, 8091 Zurich, Switzerland. E-mail address: [email protected] (C.F. Hagmann). 1 Dr Dominique Acolet sadly died before this data could be published.
neurodevelopmental delay [3,4]. The examination was subsequently reviewed and updated to form the currently used 34-item proforma. A neurological optimality scoring system was devised based on the distribution of scores for each neurological item for term-born UK infants as a means of identifying neurological optimality and sub-optimality in the early perinatal period [1]. The examination is quick and simple to perform, and can be readily learnt even by non-medical individuals [1], with good inter-rater variability [5]. The examination has been used widely for clinical and research purposes. A shortened version has been successfully tested in low-resource settings [5,6]. However to date there is no standardised study that investigates the neonatal neurological status of low-risk term-born infants in low-resource settings. This is important, as infants in low resource settings are more likely to be exposed to factors that may influence their neurological status such as infections (HIV or cytomegalovirus) during pregnancy and may have a poorer level of antenatal and intrapartum care. We found that low-risk term-born infants on the postnatal ward in a public University hospital setting in Uganda had a higher incidence of cranial ultrasound (cUS) abnormalities than
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2
C.F. Hagmann et al. / Early Human Development xxx (2015) xxx–xxx
seen in the UK population [7]. We therefore hypothesised that although apparently well and with good Apgar scores, newborn Ugandan infants would differ in their neurological exam compared to UK born infants and fewer would fall within the optimal range as defined for UK born infants. Our aim in this study was to (i) establish the range of neurological findings in apparently well newborn term Ugandan infants using our UK standardised examination, (ii) compare the findings to the published data for well term-born UK infants and (iii) to correlate their neurological findings with their perinatal characteristics and cUS imaging. 2. Methods The Institutional Review Board of the Ethics Committee, Medical School, Makerere University, Kampala, Uganda approved the study; permission from the Head of the Obstetrics Department at Mulago Hospital was also obtained. 2.1. Patients Between 24th July and 31st October 2007, 115 term infants were recruited from the postnatal wards at Mulago University Hospital, Kampala, Uganda, a major public hospital serving the general population with over 33,000 deliveries a year. Maternal informed consent was obtained by the ward nurses in the mother's own language and confirmed by the study doctors. Inclusion criteria were (i) direct admission to the postnatal ward from labour ward, (ii) gestational age (GA) ≥ 36 weeks (iii) Apgar score ≥ 8 at 5 min, and (iv) ≤ 4 days postnatal age. Antenatal and perinatal clinical details were obtained from obstetric notes and the mother. Most mothers had had some hospital based antenatal care. For the purposes of this study, women in their first pregnancy were classified as primiparous and all others were multiparous. Infants were either born by spontaneous vaginal delivery (SVD) or caesarean section (CS), which could be elective (El) or emergency (Em). ElCS was mainly done because of previous CS or a known large baby; EmCS was mainly done for failure to progress, haemorrhage, evidence for foetal stress, or cord prolapse. There was no availability of assisted delivery with forceps or vacuum extraction. 2.2. Neurological examination The infants were examined using our standardised neurological protocol [1]. Nurses familiar with the local languages were available throughout the examination; the infants were seen in a postnatal ward side-room with the mother present if she wished. FC, CH, DA, NN and NM performed the neurological examinations. NN and NM were trained by FC and DA. Initially NN and NM observed FC and DA performing the examination, scoring the examination proforma. Then “hands-on” training sessions were done and lastly, video recordings were done to evaluate the performance of NM and NN. Posters with images of each neurological item were created and posted within the side-room where the examinations took place. The results were recorded on the standard proforma containing 34 neurological items categorised into 6 groups (tone, tone patterns, reflexes, movements, abnormal signs, behaviour). Each item has a maximum of 3–5 columns arranged in a horizontal row containing a picture and/or description depicting a different response. The column that best described the infant's response or behaviour was circled. Each item was then scored from the column 1, 2, 3, 4, or 5 in which it fell. If an item fell between 2 columns, it was given the appropriate half score between the columns (e.g., items scoring between 2 and 3 scored 2.5). These scores are defined as raw scores [1]. The proforma used in the UK study (1996) was slightly different in minor ways from the proforma used in this study and the raw scores for the UK infants were amended to allow comparison to the raw scores obtained from the Ugandan infants [1].
In the UK study the distribution of the raw scores was plotted for each item and the 5th and 10th centiles were used as cutoff points. An item falling above the 10th centile was given a score of 1, between the 5–10th centiles a score of 0.5, and below the 5th centile a score of 0. A maximum score of 34 could be obtained. Scores between 30.5 and 34 were found in more than 95% of the UK study infants and were considered optimal. We applied the same process to the scores from the Ugandan infants in order to assess which scores fell in the 95th centile range for Ugandan infants and we also determined how many Ugandan infants obtained a score considered optimal for the UK population. When devising the UK system, infants were excluded if their birth GA was b37 weeks, their age at examination was outside 6–48 h, their Apgar score was b 5 after 1 min and b7 after 5 min or if their cord pH level was b 7.2. When comparing the UK and Ugandan findings the same exclusion criteria were therefore applied to the Ugandan cohort apart from cord pH as this data was not available. Birth weight was taken from the clinical notes and the head circumference was measured by us, using a disposable paper tape measure. Centiles were calculated using the LMS growth calculator (www. healthforallchildren.co.uk) from WHO2006. All infants had a cUS examination (data previously published (7)). Correlations between neurological optimality scores and cUS findings were studied. 3. Results 3.1. Patients Demographic details of the cohort are given in Table 1. Of the 115 recruited and examined infants, 96 infants were born between 37 and 42 weeks GA; 9 infants under 37 weeks GA were not included in the analysis. In ten of these 96 infants the GA was recorded only as “term age”. As there were no differences in neurological raw scores between these infants and those with a documented GA, they were analysed together. There was no statistically significant difference in median Apgar scores at 5 min between infants born by SVD, EmCs and ELCS respectively. The mean GA (SD) of the included Ugandan infants with known GA was 39.1 (±1.3) compared to 39.7 (±1.2) for the UK cohort (p = 0.001). Median Apgar scores at 1 and 5 min were 8/10 and 9/10 for the Ugandan and UK cohort respectively. There was no significant difference in birth weight (3.2 vs. 3.3 kg) or head circumference (34.9 vs. 34.5 cm) between the Ugandan and UK cohort. Fifty-six of the 96 infants were examined within 6 to 48 h of birth and of those 44 had all items scored, hence, an optimality score from those 44 could be calculated and directly compared to the UK data.
3.2. Neurological examination: raw scores 3.2.1. Correlation between raw scores, age at examination, birthweight and head circumference Although the difference was not statistically significant, infants who were examined between 48 and 96 h had higher scores than those examined before 48 h. There was no correlation between raw scores and birth weight. Infants with smaller heads performed more poorly on sucking (p b 0.01) and placing (p = 0.03) than infants with larger heads and infants with smaller heads required more consoling (p b 0.01). 3.3. Correlation between raw scores and gender Female infants had a significantly stronger leg traction response (higher score, more active tone) than male infants (p b 0.01). No other item was significantly different between male and female infants.
Please cite this article as: Hagmann CF, et al, Neonatal neurological examination in well newborn term Ugandan infants, Early Hum Dev (2015), http://dx.doi.org/10.1016/j.earlhumdev.2015.08.005
C.F. Hagmann et al. / Early Human Development xxx (2015) xxx–xxx Table 1 Maternal and neonatal demographic details. TR, mother tested and results given to the mother; TRR, mother tested and result reacted (i.e. follow-up organised); TRRDm, mother tested, results reacted and mother dosed; TRRDmDb, mother tested, results reacted and mother and baby dosed. Demographic details (n = 115) Gestational age (median (range), weeks) 35–36 weeks 37–39 weeks 40–42 weeks Term age Birth weight (median (range), grammes) Number below 3rd centile according WHO 2006 Number above 97th centile according WHO 2006 Head circumference (median (range), cm) Number below 3rd centile according WHO 2006 Number above 97th centile according WHO Females (%) Mode of delivery (%) Vaginal delivery Caesarean section (CS) Emergency CS Elective CS Unknown Apgar score at 5′ (%) 10 9 8 7 Unknown Maternal parity (%) Primigravida Multiparous Age at examination (median (range), days) HIV status (%) TR TRR TRRDm TRRDbDm Unknown
38 (35.0–42.0) 8% 55% 28% 9% 3300 (1900–4800) 4 1 35.0 (31.0–37.5) 2 0 46 59 8 16 15 2 63 12 10 4 11 44 56 2 (0–4) 76 3 1.5 1.5 18
3.4. Correlation between raw scores and maternal parity Infants born to multiparous mothers had greater passive arm recoil (p = 0.02), poorer neck extensor (p b 0.01) and flexor tone (p b 0.01) and fewer abnormal hand and toe postures (p = 0.04).
3.5. Correlation between raw scores and maternal HIV status The following items were different between infants born to HIVpositive (n = 7) and HIV-negative mothers; neck flexor and extensor tone (p b 0.01), the placing reflex (p b 0.01) and quality of spontaneous movements (p = 0.04) were all poorer in infants born to HIV-positive mothers.
3.6. Correlation between raw scores and mode of delivery Infants born by EmCS had tighter popliteal angles (p b 0.049) and less startling (p = 0.03) than those born by ElCS and by SVD.
3.7. Correlation between raw scores and cUS abnormalities The cUS findings in these infants did not correlate with any raw scores [7]. Only 3 infants had findings suggestive of haemorrhage or infarction. Cysts, either in the caudothalamic notch or the choroid plexus, were seen in 19% of the infants but these infants did not differ in terms of neurological exam from infants without these findings.
3
3.8. Neurological examination: optimality scores (n = 44) 3.8.1. Correlation between neurological optimality scores and gestational age There were no significant differences in optimality scores between infants born at 37–38 weeks, 39 to 40 weeks and those born at 41– 42 weeks GA (Table 2). Of the infants born between 39 and 40 weeks, 75% had optimal scores based on the UK data as did 60% of the infants born between 37 and 38 weeks; the 4 infants born after 41 weeks all had sub-optimal scores. 3.9. Comparison of neurological optimality scores between UK and Ugandan infants Forty-four infants had raw scores for each neurological item obtained between 6 and 48 h so that a total neurological optimality score could be calculated. The mean (SD) optimality score for the Ugandan infants was 29.7 (3.5) compared to 32.87 (1.7) for UK infants. Significantly fewer infants had an optimal score based on the UK data (N30.5) in the Ugandan cohort compared to the UK cohort (61% vs 95%). When the UK optimality scoring system was applied to infants who were examined between 48 and 96 h (n = 30), the mean optimality score was 31.20 (2.3) and 81% of the Ugandan infants had a score in the UK optimal range i.e. older infants had higher optimality scores but this difference did not reach significance. Fig. 1a–e show which items were significantly different between the British and Ugandan cohort. Fig. 2a–f illustrates the scored items of the UK and Ugandan infants. Tone items: UK infants had more flexed postures, greater passive arm and leg recoil, more active arm and leg traction, greater neck tone in flexion and extension, better attempts to raise the head in response to traction in the sitting position and greater limb flexion in ventral suspension compared to Ugandan infants. Ugandan infants had reduced hamstring tightness compared to UK infants. Tone pattern items: The Ugandan infants had significantly increased extensor tone item pattern compared to the UK infants. Reflexes: Tendon reflexes were more easily detected in the UK infants. The Ugandan infants had stronger palmar grasps. The UK infants had better placing and Moro reflex responses. Movements: UK infants exhibited significantly better quality of spontaneous movements and had better head raising responses to being placed in the prone position. Abnormal signs: Ugandan infants had significantly more abnormal hand and toe postures and less startling. Behaviour: Ugandan infants had more abnormal eye appearances. Auditory and visual orientations were better in the Ugandan infants. Ugandan infants were less irritable and required less consoling. A scoring system to identify neurological optimality and suboptimality was devised from the data from 94 term-born Ugandan infants examined within 96 h birth (Table 3). The median postnatal age of the infants at examination was 2 days. The range of total neurological scores was 27–34. Scores between 29 and 34 were found in more than 95% of the Ugandan infants and, therefore scores equal to and above 29 can be considered optimal. 4. Discussion It has been shown that neurological examination [8,9] within 6 h of birth can serve as a clinical biomarker for patient selection in cooling trials [10]. Shankaran et al reported that early neurological examination may serve as a marker for brain injury after hypoxia ischaemia as well as a response to treatment [11]. Detailed neurological examination in term infants with neonatal encephalopathy using the Hammersmith neonatal examination after the second postnatal week was predictive of neurodevelopmental outcome [12]. The lowest scores were associated with severe basal ganglia and white matter injury as seen on
Please cite this article as: Hagmann CF, et al, Neonatal neurological examination in well newborn term Ugandan infants, Early Hum Dev (2015), http://dx.doi.org/10.1016/j.earlhumdev.2015.08.005
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Table 2 Application of the UK term-born total neurological optimality scoring system to term-born Ugandan infants. Gestational age at birth
Optimality scores, mean (SD) No. (%) of infants with optimal scores No. (%) of infants with suboptimal scores
37–38 weeks (n = 20)
39–40 weeks (n = 20)
41–42 weeks (n = 4)
Total (n = 44)
29.5 (4.1) 12 (60) 8 (40)
30.25 (3.3) 15 (75) 5 (25)
28.25 (1.2) 0 (0) 4 (100)
29.73 (3.6) 27 (61) 17 (39)
magnetic resonance imaging (MRI), hence, optimality scores gave prognostic information on the severity of functional motor outcome in this population [13]. A study combining serial detailed neurological examination with brain MRI findings showed that the evolution of neurological findings (examined within 1–2 weeks, 5–7 weeks and at 6 months) is different in infants with different MR brain lesions [14]. We found a significant correlation between cUS abnormalities and neurological findings in cooled and non-cooled Ugandan infants
with perinatal asphyxial encephalopathy (unpublished data). This highlights the importance of neurological examination in clinical and in research settings. However, as we show in this study, validated optimal normative data from one population might not be applicable to another population with a different cultural background. This study presents significant differences in neurological items between the UK and the Ugandan infants. Ugandan term infants had poorer tone, poorer quality of spontaneous
Fig. 1. A. Ventral suspension. When held in ventral suspension, this infant's head was almost in line with the body and the limbs were flexed. This infant scored 3. B. Moro reflex. This infant's shoulders were abducted but there is was adduction of the arms. This infant scored 2. C. Head raising prone. Whilst in the prone position, this infant was able to lift their head but was unable to raise their chin off the bed. This infant scored 2. D. Abnormal hand or toe postures. This infant had continuous fisting and scored 4. E. Visual orientation. This infant had normal visual responses. The head turned towards the target. This infant scored 4.
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A) Tone and posture column 1
column 2
column 3
Legs slightly flexed
Leg well-flexed but not adducted
Posture
Arms & legs extended
Arm traction
Arm recoil
Arms do not flex
Arms remain straight; no resistance
↑
Head control 2
Head control 1
Popliteal angle
Leg traction
Leg recoil
No flexion
Legs straight - no resistance
↑
Arms flex slowly; not always; not completely
Arms flex slightly or some resistance felt
↑
Incomplete flexion; not every time
Legs flex slightly or some resistance felt ↑
Arms flex slowly; more complete
Arms flex well till shoulder lifts, then straighten
column 4 Leg well flexed & adducted near abdomen
Arms flex quickly and completely
column 5
Arms difficult to extend; snap back forcefully
↑
Flexion of arms <100°; mantained when body lifts up ↑
Complete but slow flexion
Complete fast flexion
Legs difficult to extend; snap back forcefully
↑
Knee flexes -well; remains flexed when bottom up ↑
1
b)
Arms flex well approx 100° & mantained as shoulder lifts ↑
Legs flex well till bottom lifts up
1 .5 2 .5 3 .5 4 .5 5
Abnormal posture: a) opistotonus
Flexion stays when back+bottom up ↑
No attempt to raise head
No attempt to raise head
Infant tries: effort better felt than seen
Infant tries: effort better felt than seen
≈ 110°
Raises head but drops forward or back
Raises head but drops forward or back
≈90°
2
1
40
1
56
Ugandan
6
<1
23
4
66
UK
46
5
39
22
9
67
UK
43
2
53
Ugandan
8
3
87
UK
35
4
44
2
6
Ugandan
15
11
69
1
2
UK
79
1
2 1
<1
8 <1
1
15
Tries to lift head but it drops back
Able to lift head slightly
Lifts head in line with body
Back curved, head ↓, limbs slightly flexed
Back slightly curved, limbs flexed
Back straight, head in line, limbs flexed
1
Ugandan
Ugandan
3
4
24
13
56
UK
1
10
1
36
2
49
Ugandan
1
4
30
17
48
UK
Head upright or extended; cannot be passively flexed
1
41
1
50
Ugandan
31
19
47
UK
61
1
9
Ugandan
6
41
14
28
UK
18
2
46
2
29
5
4
56
14
22
7
Head in front of body
5
23 12
Back curved, head & limbs hang straight
1
1
<90°
Head lag Ventral susp.
83
<1
<1
UK
5
4
Head drops & stays back
Ugandan
8
1
Raises head: remains vertical it may wobble
Raises head: remains vertical it may wobble
19
<1
7
<1
≈ 150°
4
1
5
180°
76
Back straight, head above body
1
2
Ugandan UK
Fig. 2. Distribution of raw scores in low-risk term-born Ugandan and UK infants. Each item on the proforma is illustrated by a strip as it is on the standard proforma and to the right of the strip are the percentages of Ugandan and UK infants, who score each raw score. The shading highlights the raw scores that were found in at least 10% of each subgroup. The cell with the highlighted border indicates the median score. All percentages are rounded to the nearest whole number. A. Tone and posture. B. Tone patterns. C. Reflexes. D. Movements. E. Behaviour.
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Flexor tone 1
B) Tone patterns On arm and leg traction
column 2
column 3
Arm flexion < leg flexion
Arm flexion = leg flexion
In supine
Inc. ext. tone
Neck ext. tone
Leg ext. tone
Flexor tone 2
Arms and legs generally flexed
Leg traction vs Leg traction > pop. angle than popliteal angle
Leg traction = popliteal angle
Neck in ext. vs neck in flexion
Head extension = head flexion
Vent susp vs head lag
Head extension < head flexion
Ventral suspension < head lag
Ventral suspension = head lag
column 4
column 5
Arm flexion> leg flexion but difference 1 column or <
Arm flexion > leg flexion and difference > than 1 column
Strong arm flexion with strong leg extension intermittent
Strong arm flexion with strong leg extension continuous
Leg traction < popliteal angle but difference 1 column <
Leg traction < popliteal angle and difference > than 1 column
Head extension >head flexion. but difference 1 column <
Head extension >head flexion and difference > than 1 column
Ventr suspension > head lag but difference 1 column <
Ventr suspension> head lag and difference > than 1 column
1 .5 2 .5 3 .5 4 .5 5 27
64
8
Ugandan
23
62
15
UK
Ugandan
100
99
UK
1
9
54
3
32
1
Ugandan
4
56
2
36
1
UK
8
85
6
Ugandan
5
91
5
UK
10
52
32
5
Ugandan
25
53
21
1
UK
Fig. 2 (continued).
movements, more abnormal signs including abnormal hand and toe postures compared to UK born infants. However, they showed stronger palmar grasp, better auditory and visual orientation, were less irritable and required less consoling than the UK infants. The Ugandan infants had detailed cUS and there was no correlation between cUS abnormalities and neurological findings but only very few infants had any imaging findings of definite concern (3%) [7]. Furthermore, they all had 5 minute Apgar scores in the normal range, which were not different from our UK cohort and they did not have signs of neonatal encephalopathy or other clinical problems to explain the supposed sub-optimal neurological findings. Therefore, one can speculate, that the neurological findings, which seems abnormal when compared to a UK population, may represent normal neurological findings in the Ugandan population. The Ugandan cohort was slightly younger than the UK cohort. Earlier birth gestation has been described in African populations. However we did not find a difference in neurological findings between those born at 37–38 weeks GA and those born later so the slightly earlier gestation is unlikely to be the explanation for the neurological differences we found, particularly given the good visual and auditory attention. We had found that that many infants had mild white matter echogenicity and/or sub-ependymal type cysts in the caudothalamic notch or choroid plexus cysts, the aetiology of
which was unclear. However these findings did not seem to relate to maternal HIV status [7] and these infants were not different neurologically from those without cysts. We had no evidence for maternal illness from the history we could obtain nor maternal drug intake or local herbal preparations. Hence we devised an optimality and sub-optimality scoring system for the Ugandan infants with scores of N 29 being defined as being optimal. To help validate whether these scores truly represent optimal neurological behaviour in this population development follow-up at 18–24 months should be done; however, this was not be feasible for us to do in this setting but is currently being done in another study of control Ugandan infants. Previous studies which compared the neurological examination between a UK, a Thai and Karen refugee camp cohort found that the Karen cohort had an overall decrease in tone and poorer vision performance than the British cohort [5]. They hypothesised that these differences might be associated with specific maternal nutritional deficiencies such as transketolase deficiency, which is common in that population. In a subsequent study with Vietnamese infants less marked differences in neurological items were found between the UK and the Vietnamese cohort and no correlation was found with transketolase levels [6]. Similar to the Asian infants, Ugandan infants had poorer tone compared to the UK infants, however their
Please cite this article as: Hagmann CF, et al, Neonatal neurological examination in well newborn term Ugandan infants, Early Hum Dev (2015), http://dx.doi.org/10.1016/j.earlhumdev.2015.08.005
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C) Reflexes column 1
column 2 Felt, not seen
column 3 Seen
column 4
column 5
Exaggerated
Suck/Gag
20 1
No gag / no suck
Palmar grasp
No response
Plantar grasp
No response
Moro reflex
No response or opening of hands only
Weak irregular suck only
Weak regular suck
No response
Strong suck: • irregular • regular
No suck but strong clenching
No stripping
Some stripping
Good stripping
Short, weak flexion of fingers
Strong flexion of fingers
Strong finger flexion, shoulder ↑
Partial plantar flexion of toes
Full abduction at shoulder and extension of the arms; no adduction
Dorsiflexion of ankle only
1
Very strong grasp; infant can be lifted off couch
Toes curve around the examiner’s finger
Full abduction but only delayed or partial adduction
→
Placing
1 .5 2 .5 3 .5 4 .5 5
Clonus
Tendon
Absent
2
21
76
1
5
3
2
1
1
1
3
Ugandan
<1
1
UK
91
5
Ugandan
93
2
UK
2
Ugandan
2
34
2
51
4
1
85
1
8
2
-No abduction or adduction; -Only forward extension of arms from the shoulders -Marked adduction only
3
8
6
Partial abduction at shoulder and arm extension followed by smooth adduction
71
UK
Ugandan
94 <1
97
<1
UK
8
38
4
48
1
Ugandan
1
17
3
71
8
UK
→
Full placing response with flexion of hip, knee & placing sole on surface
1 1
16 19
5
78
Ugandan
80
UK
Fig. 2 (continued).
visual and auditory orientation was better than that of the UK infants. In this study, we had no information about the maternal nutritional state. However, only three infants were small for GA, all others having age appropriate birth weight and head circumference. In the term-born UK cohort, maturation in limb and axial tone, posture and the Moro reflex was seen with increasing GA, but not in the Ugandan cohort. A reason for the lack of significant differences in the distribution of raw scores in infants born at different term GA could be the narrow range of GAs with most infants (n = 80) born between 37 and 39 weeks. Another reason could be the potential inaccuracy in determining GA of the Ugandan infants from the date of the first day of the mother's last menstrual period (LMP).
Neck flexor and extensor tone, the placing reflex and the quality of spontaneous movements were significantly poorer in Ugandan infants born to the relatively few HIV-positive mothers compared to those born to HIV-negative mothers. As the HIV status of the infants themselves was unknown, it remains speculative as to whether HIV infection had an influence on the neurological examination in these infants. However, in another study infants born to HIV positive mothers had inferior orienting scores and a greater number of abnormal reflexes on the Brazelton scale even in HIV exposed infants who do not become HIV positive [15]. HIV-infected Ugandan infants have been reported to have more motor and neurological abnormalities between 6 and 24 months of age [16]. We suggest that our neurological assessment would provide a practical tool for assessing the effects of active
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D) Movements
Movement (Quality)
Movement (Quantity)
column 1
column 2
column 3
column 4
column 5
No movement Sporadic and short isolated movements
Frequent isolated movements
Frequent generalised movements
Continuous exaggerated movements
Only stretches.
Frequent stretches and abrupt movements; some smooth movements
Fluent movements but monotonous
Fluent alternating movements of arms + legs; good variability
Cramped synchronised; mouthing jerky or other abn.mov.
Infant rolls head over, chin not raised
Infant rolls head over , raises chin
Infant brings head and chin up
Infant brings head up and keeps it up
Head raising prone
No response
1 .5 2 .5 3 .5 4 .5 5 15
81
Ugandan
4
<1
27
68
UK
7
1
73
4
<1
27
4
1
16
1
Ugandan
68
UK
42
51
2
5
Ugandan
10
50
3
37
UK
E) Abnormal signs
Startle
Tremor
Abn. hand or toe posture
column 1
No startle, even to sudden noise
column 2
column 3
column 4
column 5
Continuous fisting or thumb adduction; index finger flexion, thumb opposition
Continuous big toe extension or flexion of all toes
Hands open, toes straight most of the time
Intermittent fisting or thumb adduction
No tremor or tremor only when crying
Tremor only after Frequent Moro or tremors when occasionally awake when awake
Continuous tremors
No spontaneous startle but reacts to sudden noise
2-3 spontaneous startles
Continuous startles
More than 3 spontaneous startles
1 .5 2 .5 3 .5 4 .5 5
18
1
36
1
62
1
Ugandan
85
1
12
1
UK
89
1
7
2
Ugandan
1
UK
1
87
12
80
1
Ugandan
98
2
UK
Fig. 2 (continued).
interventions in pregnancy such as antiviral medication and antimalarials or of maternal diseases. Our observations may reflect a normal variation in the population we studied or may reflect consequences related to the minor cUS findings or the slightly earlier gestation birth or perhaps exposure to a more difficult intrauterine environment in this sub-Saharan population; it is not unreasonable to suggest that our Ugandan population may represent populations in much of Africa. The findings provide baseline data for comparison with neurological examination from sick infants from similar communities at risk of impaired neurodevelopmental outcomes such as preterm infants and/or term infants with neonatal encephalopathy or seizures. The data are also important for studies or trials of neonatal treatments in which neurological examination will be used to select for neuroprotective studies, to assess progress of disease and predict outcome.
Conflict of interest statement There is no conflict of interest.
Funding This project was initiated as part of the Uganda Women's Health Initiative (UWHI) involving the University College London, Institute for Women's Health, Mulago Hospital, Makerere University and Hospice Africa Uganda. We are grateful to Professor Ian Jacobs and Dr Anthony Gakwaya co-directors of UWHI and Mr Graham Evans project manager of UWHI for their support and guidance. The UWHI and this project were supported by generous donations from Lee and Roger Myers and Ann-Margaret and John Walton.
Please cite this article as: Hagmann CF, et al, Neonatal neurological examination in well newborn term Ugandan infants, Early Hum Dev (2015), http://dx.doi.org/10.1016/j.earlhumdev.2015.08.005
C.F. Hagmann et al. / Early Human Development xxx (2015) xxx–xxx
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F) Behaviour Eye movements
column 1
column 2
Does not open eyes
Full conjugated eye movements
Visuaal orientation Alertness Irritability
column 4
column 5
Transient -nystagmus -strabismus -roving eye mov. -sunset sign
Persistent -nystagmus -strabismus -roving eye mov. -downward deviation
Auditory startle; brightens and stills; no true orientation
Shifting of eyes, head might turn towards source
Prolonged head turn to stimulus; search with eyes; smooth
Turns head and eyes towards noise every time; jerky abrupt
Does not follow or focus on stimuli
Stills, focuses, follows briefly to the side but loses stimuli
Follows horizontally and vertically; no head turn
Follows horizontally and vertically; turns head
Follows in a circle
Will not respond to stimuli
When awake, looks only briefly
When awake, looks at stimuli but loses them
Keeps interest in Does not tire stimuli (hyper-reactive)
Quiet all the time, not irritable to any stimuli
Awakes, cries Cries often sometimes when when handled handled
Cries always when handled
Asleep; awake, no crying; consoling not needed
Awake; cries briefly; consoling not needed
Awake; cries; becomes quiet when talked to
Awake; cries ; needs picking up to console
No cry at all
Whimpering cry only
Cries to stimuli but normal pitch
Auditory orientation
No reaction
1 .5 2 .5 3 .5 4 .5 5 1
96
3
Ugand an
8
92
<1
UK
1
1
10
1
51
4
33
Ugandan
24
6
50
5
15
UK
2 8
Cries even when not handled
Awake; cries cannot be consoled
High pitched cry; often continuous
17 2
14 12
Cry
Consolability
column 3
3
79
6
60
5
50
7
27
2
1
21
Ugandan
3
UK
37
4
47
38
1
47
38
2
44
2
UK
4
1
Ugandan
12 1
59
Ugandan
26
2
5
UK
28
4
12
Ugandan
52
2
12
UK
1
99
Ugandan
5
95
UK
Fig. 2 (continued).
Table 3 Compound optimality scores for the Ugandan total neurological optimality scoring system.
Tone and posture Tone patterns Reflexes Movements Abnormal signs Behaviour
Range of compound scores
Range of optimal compound optimality scores
Suboptimal compound optimality scores
6–10 3–5 3.5–6 1–3 1–3 4.5–7
8–10 4.5–5 5–6 2.5–3 2.5–3 6–7
b8 b4.5 b5 b2.5 b2.5 b6
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Appendix A Differences between the 1996 proforma on which the neurological examination results of the UK infants were recorded and the 2007 proforma on which the neurological examination results of the Ugandan results were recorded. Raw scores for the UK data were amended as shown below to match the 2007 proforma. A.1. Leg extensor tone Amendments to UK raw data: raw scores of 2 and 4 were switched.
1996
Leg traction vs pop. angle
2007
Leg traction vs pop. angle
Column 2
Column 3
Column 4
Column 5
Leg traction b popliteal angle but difference 1 column b Leg traction N than popliteal angle
Leg traction = popliteal angle
Leg traction N than popliteal angle
Leg traction = popliteal angle
Leg traction b popliteal angle but difference 1 column b
Leg traction b popliteal angle and difference N than 1 column Leg traction b popliteal angle and difference N than 1 column
A.2. Suck/gag Amendments to UK raw data: raw scores of 2 were re-scored to 3 or remained as 2, raw scores of 3 became 4, and raw scores of 4 became 5. 1996
2007
Column 1
Column 2
Column 3
Column 4
No gag/no suck
Weak suck only: ● Irregular ●Regular No stripping Weak irregular suck only No stripping
Strong suck: ● Irregular ● Regular Good stripping Weak regular suck Some stripping
No suck but strong clenching
No gag/no suck
No suck but strong clenching
Strong suck: ● Irregular ● Regular Good stripping
A.3. Spontaneous movements Amendments to UK raw data: raw scores for spontaneous movement became the raw scores for movement (quantity) and movement (quality).
1996
Column 1
Column 2
Column 3
Column 4
Column 5
No movement
Few stretches, no other movement, smooth movement
Smooth movement some jerky movement + stretches
Smooth alternating movements of arms + legs
Fits, or other abnormal movements, describe
Frequent isolated movements
Frequent generalised movements
Continuous exaggerated movements
Fluent movements but monotonous
Fluent alternating movements of arms + legs; good variability
Cramped synchronised; mouthing jerky or other abn.mov.
Spontaneous movement (quantity) 2007 No movement Sporadic and short isolated movements Spontaneous movement (quality) 2007 Only stretches. Frequent stretches and abrupt movements; some smooth movements
A.4. Abnormal hand or toe postures Amendments to UK raw data: raw scores of 1 became 2, raw scores of 2 became 3, raw scores of 3 became 4, and raw scores of 4 became 5.
1996
Column 1
Column 2
Column 3
Column 4
Hands open
Hands fist or thumbs adduct but opens Hands open, toes straight most of the time
Hands fist or thumb adducts, finger & thumb oppose always Intermittent fisting or thumb adduction
Big toe up (extends) or all toes flex always
2007
Column 5
Continuous fisting or thumb adduction; index finger flexion, thumb opposition
Continuous big toe extension or flexion of all toes
A.5. Tremor Amendments to UK raw scores: raw scores of 1 became 2, raw scores of 4 became 3, and raw scores of 4.5 became 5. Column 2
Column 3
Column 4
Column 5
1996 No tremor Tremor only when crying Tremor only after Moro Some tremor when awake Lots of tremor when awake 2007 No tremor or tremor only when crying Tremor only after Moro or occasionally when awake Frequent tremors when awake Continuous tremors
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C.F. Hagmann et al. / Early Human Development xxx (2015) xxx–xxx
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A.6. Eye movements Amendments to UK raw scores: raw scores of 2 became 3, and raw scores of 3 became 4 or 5.
1996 2007
Column 1
Column 2
Column 3
Does not open eyes Does not open eyes
Normal eye movement, eyes move together
Abnormal eye movements, describe Full conjugated eye movements
Column 4
Column 5
Transient –Nystagmus –Strabismus –Roving eye mov.
Persistent –Sunset sign –Nystagmus –Strabismus –Roving eye mov. –Downward deviation
A.7. Irritability Peak of excitement and irritability were incorporated into one item, irritability. Amendments to UK raw scores: an average of the raw scores for peak of excitement and irritability were used as the raw score for the revised irritability item. Peak of excitement (Circle ‘H’ if high pitch cry). Column 1
Column 2
Column 3
Column 4
Column 5
Quiet all the time H
Awakes briefly, does not cry H
Awakes briefly, cries sometimes H
Cries always when handled H
Cries always H
Irritability 1996 Not irritable to stimuli
Cries 1–2 times
Cries 3–4 times
Cries to all stimuli
Cries even when not handled
Irritability 2007 Quiet all the time, not irritable to any stimuli
Awakes, cries sometimes when handled
Cries often when handled
Cries always when handled
Cries even when not handled
1996
A.8. Cry This item was not present in the 1997 proforma. Amendments to UK raw scores: Infants with a raw score of 1 for Peak of excitement and Irritability on the 1997 proformas, retained their raw score of 1. Infants whose cry was recorded as high-pitched on the Peak of excitement item were given a raw score of 5. The remaining infants were given a new raw score of 3.
2007
Column 1
Column 2
Column 3
No cry at all
Whimpering cry only
Cries to stimuli but normal pitch
References [1] Dubowitz L, Mercuri E, Dubowitz V. An optimality score for the neurologic examination of the term newborn. J Pediatr 1998;133(3):406–16. [2] Dubowitz LM, Dubowitz V, Palmer P, Verghote M. A new approach to the neurological assessment of the preterm and full-term newborn infant. Brain Dev 1980;2(1): 3–14. [3] Haataja L, Mercuri E, Cowan F, Dubowitz L. Cranial ultrasound abnormalities in full term infants in a postnatal ward: outcome at 12 and 18 months. Arch Dis Child Fetal Neonatal Ed 2000;82(2):F128–33. [4] Haataja L, Mercuri E, Regev R, Cowan F, Rutherford M, Dubowitz V, et al. Optimality score for the neurologic examination of the infant at 12 and 18 months of age. J Pediatr 1999;135(2 Pt 1):153–61. [5] McGready R, Simpson J, Panyavudhikrai S, Loo S, Mercuri E, Haataja L, et al. Neonatal neurological testing in resource-poor settings. Ann Trop Paediatr 2000;20(4): 323–36. [6] Hieu NT, Gainsborough M, Simpson JA, Thuy NT, Hang NN, Taylor AM, et al. Neurological status of low-risk Vietnamese newborns: a comparison with a British newborn cohort. J Health Popul Nutr 2006;24(1):57–63. [7] Hagmann CF, Robertson NJ, Acolet D, Chan D, Onda S, Nyombi N, et al. Cranial ultrasound findings in well newborn Ugandan infants. Arch Dis Child Fetal Neonatal Ed 2010;95(5):F338–44. [8] Sarnat HB, Sarnat MS. Neonatal encephalopathy following fetal distress. A clinical and electroencephalographic study. Arch Neurol 1976;33(10):696–705.
Column 4
Column 5 High pitched cry; often continuous
[9] Thompson CM, Puterman AS, Linley LL, Hann FM, van der Elst CW, Molteno CD, et al. The value of a scoring system for hypoxic ischaemic encephalopathy in predicting neurodevelopmental outcome. Acta Paediatr 1997;86(7):757–61. [10] Gunn AJ, Wyatt JS, Whitelaw A, Barks J, Azzopardi D, Ballard R, et al. Therapeutic hypothermia changes the prognostic value of clinical evaluation of neonatal encephalopathy. J Pediatr 2008;152(1):55–8 [8 e1]. [11] Shankaran S, Laptook AR, Tyson JE, Ehrenkranz RA, Bann CM, Das A, et al. Evolution of encephalopathy during whole body hypothermia for neonatal hypoxic-ischemic encephalopathy. J Pediatr 2012;160(4):567–72 [e3]. [12] Mercuri E, Guzzetta A, Haataja L, Cowan F, Rutherford M, Counsell S, et al. Neonatal neurological examination in infants with hypoxic ischaemic encephalopathy: correlation with MRI findings. Neuropediatrics 1999;30(2):83–9. [13] Haataja L, Mercuri E, Guzzetta A, Rutherford M, Counsell S, Flavia Frisone M, et al. Neurologic examination in infants with hypoxic-ischemic encephalopathy at age 9 to 14 months: use of optimality scores and correlation with magnetic resonance imaging findings. J Pediatr 2001;138(3):332–7. [14] Ricci D, Guzzetta A, Cowan F, Haataja L, Rutherford M, Dubowitz L, et al. Sequential neurological examinations in infants with neonatal encephalopathy and low Apgar scores: relationship with brain MRI. Neuropediatrics 2006;37(3):148–53. [15] Scafidi F, Field T. Brief report: HIV-exposed newborns show inferior orienting and abnormal reflexes on the Brazelton Scale. J Pediatr Psychol 1997;22(1):105–12. [16] Drotar D, Olness K, Wiznitzer M, Guay L, Marum L, Svilar G, et al. Neurodevelopmental outcomes of Ugandan infants with human immunodeficiency virus type 1 infection. Pediatrics 1997;100(1):E5.
Please cite this article as: Hagmann CF, et al, Neonatal neurological examination in well newborn term Ugandan infants, Early Hum Dev (2015), http://dx.doi.org/10.1016/j.earlhumdev.2015.08.005