Early Human Development, 24 (1990) 93-105 Elsevier Scientific Publishers Ireland Ltd.
93
EHD 01095
Postural development in very low birth weight and normal birth weight infants Christopher Molteno=, Vivien Magasinera, Rauf Sayed” and Michael Karplusb *Departments of Paediatrics and Child Health and Community Health, University of Cape Town Cape Town and Red Cross War Memorial Children’s Hospital, Rondebosch (South Africa) and bDepartment of Pediatrics, Soroka Medical Centre, Ben-Gurion, University of Negev, Beer-Shelva (Israel) (Received 2 August 1988; revision received 19 June 1990, accepted 17 July 1990)
Summary In this study the seven postural responses selected by Vojta to evaluate neuromotor development were applied to 68 very low birth weight (VLBW) (> 1500 g) infants and to 28 healthy infants of normal birth weight (< 2500 g). Of the 68 VLBW infants, 41 were small for gestational age and 27 appropriate for gestational age. All infants were examined between 37 and 40 weeks postmenstrual age. They were all later assessed on the Griffiths Mental Developmental Scale at 12 and 18 months. There were significant differences in postural reactions between the two groups which confirmed the lower tone and greater extension previously described in very low birth weight infants. An important finding in the study was that poor head and trunk righting noted at four months corrected age in very low birth weight infants, was associated with less developed locomotion at 12 and 18 months as assessed by the Griffiths Mental Developmental Scale. Thus, a delay in maturation in very low birth weight infants which was apparent from the assessment of postural responses in early infancy was still identifiable on the locomotor subscales at 12 and 18 months. Five of Vojta’s responses were shown to be useful as part of the neurological assessment of high risk infants. postural responses; very low birth weight infants; locomotor development.
Correspondence to: Dr C.D. Molteno, University of South Florida, Department of Pediatrics, Box 15, 12901 Bruce B Downs Blvd., Tampa, Florida 33612-4799, U.S.A. 0378-3782/90/.$03.50 @ 1990 Elsevier Scientific Publishers Ireland Ltd. Published and Printed in Ireland
Introduction The improved quality of neonatal intensive care has greatly enhanced the chances of survival of infants who would otherwise have died. The survivors have, unfortunately, a higher risk of long term neurodevelopmental handicap. In Sweden [8] a decline in incidence of cerebral palsy was reported for the period 1954-1970, but from 1971-1978 it was found to have increased. More recently, Hagberg et al. [9] have reported a further rise in the incidence of cerebral palsy associated with a parallel decrease in perinatal mortality, especially in preterm infants. Stanley [ZO] has shown that there has been a marked fall in perinatal mortality in Western Australia with an increase in the rate of cerebral palsy among very low birth weight (VLBW) infants from 14.0/1000 live births in 1%8-1971 to 25.0/1000 in 1979-1981. In the first period (1968-1971) only 5.3% of all children with cerebral palsy had been less than 1500 g birth weight but this had risen to 11.5% in the years 1979-1981. In contrast, Haas et al. [7] reported an improved outcome in VLBW infants from 1977 to 1983. The incidence of neurological sequelae in their study declined from 9.2% in 1977-1979 to 3.7% in 1982-1983. The evaluation of neuromotor development is a valuable part of the neurological assessment of infants and this is particularly important in the follow up of all VLBW babies. It is known that the motor pattern of the VLBW infant differs from that of the full term, but existing tests do not serve to differentiate those babies who are neurologically normal in the longterm from those who are neurologically impaired. In 1976 Vojta [21] selected seven ‘postural reactions’ of normal, healthy infants in order to evaluate neuromotor development according to age. Deviations from the normal patterns could be considered as either ‘delayed’ or ‘pathological’. We felt that it would be useful to document the postural responses in VLBW infants. The aims of the study were (1) to investigate whether the motor patterns as determined by postural responses selected by Vojta differed between VLBW, AGA and SGA infants and controls at full term and follow-up and (2) to determine whether deviations detected by this examination technique would help in the early detection of cerebral palsy. Matprials and Methods Between August 1984 and June 1985, 68 VLBW (birth weight < 1500 g) and 28 healthy full term infants of normal birth weight (> 2500 g) were selected for study. The VLBW infants consisted of 41 smaIl for gestational age (SGA) (less than 10th centile using Lubchenco charts [l]) and 27 appropriate for gestational age (AGA) white and coloured (mixed ancestry) infants born in the Peninsula Maternal and Neonatal Service, which forms part of the University of Cape Town teaching hospitals. Gestational age was assessed by the method of Dubowitz et al. [3]. All infants, both VLBW and full term infants of normal birth weight (referred to as full term infants), were tested for postural reactions as specified by Vojta. Two VLBW and one full term infant were selected each week. If there were more than two VLBW infants available, those with the lowest birth weights and gestational
95 TABLE I Birthweight. gestational age, delivery and Apgar Scores in VLBW and full-term infants. Full-term
VLBW SGA
AGA
Number
41
21
28
Birthweight (g) S.D.
lux) 245
1299 118
3330 130
Gestational age (weeks) SD.
33.8 2.3
30.7 1.7
38.9 0.86
;:4%) 21
13 (48 qo) 14
28 (100%)
5.3 2.6 7.6 2.3
5.9 2.1 8.0 1.7
8.96 0.48 9.93 0.07
Delivery SVD Other Apgar Scores 1 min SD. 5min S.D.
‘SVD = spontaneous vertex delivery.
ages were enrolled in the study and examined between 37 and 40 weeks post menstrual age. The full term infants who were all examined on or after the second day of life (mean 3.7 days) were well grown, born by normal vertex deliveries, following normal pregnancies. They all established sustained respiration spontaneously after delivery and had unconplicated neonatal courses. Details of the infants are given in Table I. At the time of the first examination the mean weight of the VLBW infants was 1940 g, S.D. 240 and for the full term infants it was 3105 g, S.D. 534. The social backgrounds of all the infants were assessed on the ‘levels of living’ of Riley et al. [ 171, which are based on parental education and occupation and family income and housing density. This assessment has been compiled for the city of Cape Town using census data and yields scores of O-60, with the lower scores being most favourable. A pilot study involving 40 infants examined at term and four months was carried out prior to August 1984 and an evaluation chart was drawn up. All assessments were carried out by V.M.* in the nursery midway between feeds. A second identical evaluation of postural reactions was conducted at four months corrected age, i.e., 40 weeks post menstrual age plus 16 weeks (f 3 days). One *V.M. spent 3 weeks in the Department of Neonatology at Soroka Hospital, Beer Sheva, Israel under the supervision of M.K. V.M. became familiar with the evaluation of the postural responses and prepared a chart for recording the responses.
96
VLBW infant was not assessed at four months because of illness. At 12 and 18 months corrected age all infants were assessed by C.M. using the Griffiths Scales of Mental Development [2]. Assessment of postural reactions
(9
Traction response. With the infant supine, traction was applied to both arms until the trunk formed an angle of 45’ with the examination plane. The degree of head lag, arm flexion and position of the legs was noted.
(ii)
Landau response. The infant was held in a horizontal position with the examiner’s hand supporting the lower chest and upper abdomen. The position of the head, spinal curvature and degree of flexion of arms and legs was noted.
(iii)
Axillary hanging. The infant was held from behind, below the axillae and suspended vertically with the feet just clear of the table. Care was taken not to exert pressure on the back, which could have stimulated trunk extension. The position of the head and legs was noted.
(iv)
Side tilting according to Vojta. The infant was held vertically with the back to the examiner and tilted suddenly into the lateral horizontal position. The position of the head, trunk, upper arms and both legs was noted.
(v)
Collis horizontal suspension. With the infant lying on one side and the back to the examiner, the uppermost shoulder and hip joints were grasped, taking hold of the whole joint thus avoiding stretching the ligaments. The infant was then lifted just off the table. The positions of the head, trunk and free arm and leg were noted.
(vi)
Peiper response. The infant was placed supine with the head in the midline to prevent the influence of an ATNR. The examiner grasped the legs at the level of the knees, lifting the infant suddenly into inverted vertical suspension. The position of the head, trunk, arms and hands was noted.
(vii)
Collis vertical response. Following the Peiper response with the infant still in the vertical position, one leg was released and the position it took was noted. This leg was then grasped again and the same procedure was repeated with the other leg.
The behavioural state of the infant was recorded for each reaction. Four states were recognized - sleepy, awake with eyes open and minimal movement, awake and irritable or fussing and crying. All the results were recorded on a prescribed proforma and entered for computer analysis. The Chi-squared and the Fishers’ exact tests were used to test the differences between VLBW and full term infants for each of the postural reactions, and also the association between the assessment of pos-
97
tural reactions and locomotion. Student’s t-test.
Developmental quotients were compared using the
Results Postural responses and state at term The comparison of the postural reactions in the VLBW infants (corrected for prematurity) and the full term infants is shown in Table II. The VLBW infants tended to have lower tone and were more extended than the full term infants. On the traction response, the VLBW infants had significantly more head lag although many of the full term infants had more head lag than expected. One VLBW infant had a limp head drop which constitutes an abnormal response. The VLBW infants had less hip flexion, but there was no difference in arm flexion between the two groups. The Landau showed the VLBW infants to have more extension of head, trunk, arms and legs than the full term infants. On axillary hanging there was no difference in head posture, but the legs of the VLBW infants were more extended. The Vojta side tilting demonstrated more extension of the upper leg in the VLBW infants although there was no difference in head and trunk or arm posture. Similarly the Collis horizontal showed more extension of the VLBW infants’ legs only. There were no differences between the two groups on either the Peiper or the Collis vertical response. Regarding the state, the full term infants cried more during the Vojta (P < O.OOl),Collis horizontal (P< O.Ol), Peiper and Collis vertical (P< 0.001) response. Postural responses and state at four months At four months corrected age the VLBW still had more head lag than the full term infants on the traction response. They also had more arm extension and less hip flexion than the full term infants (Table II). There were no differences between the two groups on the Landau or the axillary hanging. The Vojta and Collis horizontal both showed the VLBW infants to have significantly less head and trunk righting responses than the full term infants. The two groups did not differ on the Peiper or Collis vertical reactions. There were no significant differences in state at four months. In both the term and four month assessments a number of full term infants had responses considered deviant by Vojta [19]. For example, at term 21.4% held their arms in suspension during the Landau and 17.9% had initial leg extension during axillary hanging. At four months a quarter still showed head lag and 42.8% arm extension on the traction response. These responses would have been more typical of VLBW infants. Comparison of AGA and SGA infants corrected to term andfour months There were no significant differences between SGA and AGA VLBW infants at 40 weeks post menstrual age. The SGA infants at four months corrected age had less head control on the traction response (P < 0.05) and cried more during the Vojta side tilting (P < 0.05) than the AGA infants.
58.8 41.2
Head flexed. trunk slightly curved P
%
Y/N
%
25.0
75.0
Head flexed, trunk curved
Elbow flex P
Elbow ext
Hip and knee in strong flex P
Qcl
G
Y-+/L
Hip and knee ext then flex or Hip in maximum abd. knee flex
Hip and knee in moderate flex
%
5.9
Moderate head lag
Full head control P
94.1
< 0.01
< 0.001
< 0.005
14.3
85.7
92.9
7.1
32.1
67.9
41.2
58.8
69.1
17.7
13.2
41.2
58.8
< 0.005
< 0.001
< 0.001
VLBW %
VLBW % Full-term %
4 months corrected age
0 months corrected age
Traction Marked head lag
Postural responses (significant results only).
TABLE II
78.6
21.4
loo.0
89.3
10.7
%
Full-term
99
E; d
V
9-9
Abbreviations: Flex, flexion; Ext, extension; Abd, abduction.
Hip and knee in ext then flex P
Hip and knee in loose flex
Righting of head, neck and trunk P
Collishorizontal Suspension of head, neck and trunk
TABLE II (continued)
25.0
58.8 < 0.01
75.0
41.2
67.6
32.4
< 0.005
VLBW %
VLBW %
Full-term %
4 months corrected age
0 months corrected age
100.0
Full-term 070
8
101 TABLE III Griffiths assessments at 12 and 18 months (mean f S.D.) Full-term n = 28
VLBW n = 68
106f
101 *
P value
I2 Months
Development quotient Sub-scale quotients Locomotion Personal/Social Hearing/speech Eye/hand Performance 18 Months Development quotient Sub-scale quotients Locomotion Personal/social Hearing/speech Eye/hand Performance
8
110 + 13 104* 5 103k 7 106* 7 108 + 10
1042
8
0.001
104f 13 101 f 8 101 + 11 101 f 7 98k 9
0.025 NS NS 0.003 0.001
6
992
8
0.002
104 + 10 101 + 6 104 f 10 103* 7 107+ 6
100 f 96 f 97 f 1002 102 f
13 10 12 8 10
0.015 0.015 NS 0.02
NS
Assessment at 12 and 18 months corrected age The VLBW infants performed less well on the Griffiths assessment at 12 and 18 months (Table III). Regarding the subtests, significant differences were found at 12 months in locomotion, eye-hand coordination and performance and at 18 months in personal/social, hearing and speech and performance. Three VLBW infants had neuro-developmental handicap (evidence of cerebral palsy and/or a DQ < 80). One had mild spastic diplegia and a normal DQ, a second spastic quadriplegia and a DQ of 65 and the third a DQ of 69 at 12 months. Cross correlation of the postural responses at term with DQs at 12 months revealed significances with arm extension bilaterally on the Landau response. There were no other significant associations between postural development and DQ at 12 or 18 months. However, associations were found between the locomotor subtests and postural responses. Extended arms on the Landau at 0 months corrected age in VLBW infants was associated with more advanced locomotor development at 12 months (P < 0.05). An open right hand in the Vojta side tilting at term corrected age was also associated with enhanced locomotion at both 12 and 18 months (P< 0.05). At four months corrected age delayed head and trunk righting on the left side in the Vojta side tilting was associated with a lower locomotor score at 12 and 18 months (P < 0.05). At four months corrected age delayed head and trunk righting on the right side in the Collis horizontal was associated with a lower locomotor score at 12 and 18 months (P < 0.05). Abduction of the shoulder with elbow flexion during the Peiper response was associated with more delayed locomotor development at 12 (P < 0.01) and 18 months (P < 0.03). The infants who cried more during the Landau, axillary hanging and Vojta at four
102
months corrected age performed less well on the locomotor subtest at 12 and 18 months (P < 0.05). Although all infants were drawn from the same hospital delivery population, the social backgrounds of the VLBW ‘infants (level of living scores, mean 35.6, SD. 26) were significantly less favourable than those of the full term infants (level of living scores, mean20, SD. 15.9; t = 3.88, P< 0.01). Discussion The assessment of postural reactions described by Vojta [21] was designed for the diagnosis of cerebral motor dysfunction. Noren and Franzen [14] tested 25 healthy infants from the newborn period to 18 months and found a considerable number of deviations from normal/optimal as specified by Vojta. The Vojta response yielded the highest number of deviations and the traction response the lowest, with the largest number noted at three months and the least in the newborn period. They did not specify the types of deviation. Hellstrom et al. [lo] found the traction response from 2 to 12 months frequently differed from that expected according to the description of Vojta, whereas the Landau and Collis vertical reactions followed, with a few exceptions, those expected for age. Japanese infants tested by Yumori et al. [22] were noted to have a tendency towards extensor reactions on the axillary hanging, Landau, Vojta, Collis horizontal and Collis vertical responses. Our full term infants also had a number of deviations from the expected responses, both at term and four months. Most of the deviations involved extension of the limbs which would have been more typical of the VLBW infants. The postural responses as specified by Vojta have not, to our knowledge, been applied to low birth weight infants. The first aim of the study was to compare the postural responses of VLBW, AGA and SGA infants and controls at full term and follow-up.There were significant differences in tone and degree of flexion between VLBW and full term infants. SaintAnne-Dargassies [18] found former premature infants to have less passive tone with wider angles and dangling of a larger amplitude than full term infants. The ex-premature infant also exhibited movements of greater amplitude and more varied, but they tended totire sooner. She put forward two possible explanations for the difference. Firstly, the full term infants had been more compressed in utero with their limbs being increasingly flexed in an elastic liquid milieu which was constantly dwindling and secondly, the ex-premature infants were generally less optimally nourished. The finding of lower tone and less flexion of VLBW infants also agrees with Palmer et al. [4] and with Howard et al. [l 11, who reported weaker responses especially on items involving muscle tone in premature infants. They were also more difficult to soothe. Forslund and Bjerre [5] found preterm infants to have lower muscle tone as judged by spontaneous posture of arms and legs, poor resistance to passive movements and slow arm recoil. In the traction test they had more head lag. Similarly, Kurtzberg et al. [12] reported lower tone in LBW infants, a higher incidence of crying following aversive items and a longer mean consolation latency. Our full term infants in contrast cried more during four of the seven responses. Brown [2] asso-
103
ciates motor development with sub-cortical brain maturation. He divides motor development into four stages, a first flexor and first extensor stage followed by a second flexor and extensor stage. The extension of the preterm infant could be associated with a prolonged secondary extensor developmental stage. Sarnat [I91has related the sequence of myelination to the changes in posture of the premature infant with advancing conceptional age. Prechtl and Nolte [I61 introduced a further variable, the differences in body weight which could affect muscle power. The VLBW infants in our study were still markedly underweight when compared to full term infants. The Griffiths Scales of Mental Development have been used by Goodman et al. [4] in VLBW follow up. At 12 months the locomotion subscales in both of their study groups (viz. ‘at risk’ and ‘normal’ VLBW infants) were higher than the other subscales. In our study the locomotion subscales in both VLBW and control groups were higher than other subscales at 12 but not at 18 months. The social disadvantage of the VLBW infants could have accounted for some of the developmental differences at follow-up. McCall [13], however, has postulated that mental development early in life, especially up until 18 to 24 months, is strongly canalized and slowly becomes less strongly canalized thereafter. Both genetic and environmental factors have minor correlations with mental performance before 18 to 24 months and both have increasing correlations after 24 months. Thus, although social class may have accounted for some of the differences in the personal/social and hearing/speech subtests at 18 months, social background is unlikely to have been responsible for the developmental differences at 12 months, which were on the locomotion, eye/hand and performance subtests. Regarding the second aim, to determine whether deviations detected by examining postural responses would help in the early detection of cerebral palsy, only two of the VLBW infants developed cerebral palsy - one a mild diplegia and the other a more severe spastic quadriplegia with general developmental delay. The child with diplegia showed no abnormal postures at term or at four months corrected age. The quadriplegic had no abnormal postures at term corrected age but unfortunately was ill at four months and was not examined. A greater number of cerebral palsied children would be needed to determine whether postural responses are useful in the early detection of cerebral palsy, but the limited findings of this study would not support it. The development of head and trunk righting distinguished VLBW from full term infants and also correlated with subsequent locomotor performance. The progress of head and trunk righting from birth to four months was particularly well demonstrated in the Vojta and Collis horizontal responses. Similarly, there was good correlation between head and trunk righting at four months on the Vojta and Collis horizontal responses and locomotion at both 12 and 18 months, suggesting a persisting maturational delay, although the locomotion subtest quotients for both the preterm and term infants were still within normal limits. Poor head and trunk righting is a strong indication of lack of trunk control which is a requirement for gross motor development. The statistical significance of the association between head and trunk righting and locomotor scores is important and warrants further attention.
104
In conclusion, the seven postural reactions selected by Vojta brought out significant differences between VLBW and full term infants at term corrected age. These differences related especially to lower tone and less flexion in VLBW infants. By four months the leg extension of the VLBW infants was no longer present, although delay in head and trunk control persisted. The head lag on the traction response was more marked in SGA than AGA infants. Head and trunk righting at four months was also related to locomotor development at 12 and 18 months as assessed by the Griffiths Scales of Mental Development. The postural responses are therefore useful in assessing aspects of VLBW infant development. Although this study was not helpful in detecting signs of later neurological abnormality, as a result of the study, a neurodevelopmental assessment chart was prepared. The chart combined the first five of Vojta’s postural responses together with an assessment of specific primitive reflexes and passive muscle tone. This chart is proving successful clinically and is being evaluated on a group of high risk VLBW infants with significant intraventricular haemorrhages. References 1 2 3 4
5 6 7
12
13
14 15
Battaglia, F. and Lubchenco, L. (1%7): A practical classification of newborn infants by weight for gestational age. J. Pediatr., 71, 159-163. Brown, J.K. (1974): General Neurology. In: Neonatal Medicine, p. 522. Editors: F. Cockburn and C. Drillien. Blackwell Scientific Publications, Edinburgh. Dubowitz, L.M.S., Dubowitz, V. and Goldberg C. (1970): Clinical assessment of gestational age in the newborninfant. J. Pediatr., 77, l-10. Goodman, M., Rothberg, A.D., Houston-McMilIan, J.E., Cooper, P.A., Cartwright, J.D. and Van der Velde, M.A. (1985): Effect of early neurodevelopmental therapy in normal and at-risk survivors of neonatal intensive care. Lancet, ii, 1327-1330. Forslund, M. and Bjerre, I. (1983): Neurological assessment of preterm infants at term conceptual age in comparison with normal full-term infants. Early Hum. Dev., 8, 195-208. Griffiths, R. (1976): The Abilities of Babies. A Study in Mental Measurement. Association for Research in Infant and Child Development, Amersham. Haas, G., Buchwald-Aal, M., Ledig, E. and Mentzel, H. (1986): Improved outcome in very low birth-weight infants from 1977-1983. Eur. J. Pediatr., 145,337-340. Hagberg, B., Hagberg, G. and Olow, I. (1984): The changing panorama of cerebral palsy - Sweden, 1959-1978. Acta Paediatr. Stand., 73,433-440. Hagberg, B., Hagberg, G., Olow, I. and von Wendt, L. (1989): The changing panorama of cerebral palsy in Sweden. V. The birth year period 1979-82. Acta Paediatr. Stand., 78,283-290. Hellstrom, B., Knutsson, E. and Wessman, A. (1982): The traction reaction in infancy - clinical and electromyographic study of normal infants. Neuropediatrics, 13,63-71. Howard, J., Parmelee, A.H., Kopp, C.B. and Littman, B.A. (1976): Neurologic comparison of preterm and full-term infants at term conceptional age. J. Pediatr., 88,995-1002. Kurtzburg, D.. Vaughan, H.G., Daum, C., Grellong, B.A., Albin, S. and Rotkin, L. (1979): Neurobehavioural performance of low birthweight infants at 40 weeks conceptional age: comparison with normal full-term infants. Dev. Med. Child Neurol., 21, 590-607. McCall, R. (1979): The Development of Intellectual Functioning in Infancy and the Prediction of Later IQ. In: Handbook of Infant Development, p. 732. Editor: J. Osofsky. John Wiley and Sons, New York. Noren, L. and Franzen, G. (1981): An evaluation of seven postural reactions (‘Lagereflexe’ selected by Vojta) in twenty five healthy infants. Neuropediatrics, 12, 308-312. Palmer, P.G., Dubowitz, L.M.S., Verghote, M. and Dubowitz, V. (1982): Neurological and neuro-
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16
17
18 19 20 21 22
behavioural differences between preterm infants at term and full-term newborn infants. Neuropediatrics, 13, 183-189. Prechtl, H.F. and Nolte. R. (1984): Motor behavior in preterm infants. In: Continuity of Neural Function from Prenatal to Postnatal Life. Clinics in Developmental Medicine, No. 94, p. 79. Editor: H.F.R. Prechtl, London S.I.M.P. with Blackwell Scientific, Philadelphia, Lippincott. Riley, N., Schuman. C., Romanowsky, P. and Gentle, R. (1984): Spatial Variations in the Levels of Living in the Cape Metropolitan Area. Second Inquiry into Poverty and Development in Southern Africa. Conference Paper No. 13, University of Cape Town, April. Saint-Anne Dargassies, S. (1977): Neurological Development in the Full-Term and Premature Neonate, pp. 222-224. Excerpta Medica, Amsterdam. Samat, H.B. (1984): Anatomic and Physiologic Correlates of Neurologic Development in Prematurity. In: Topics in Neonatal Neurology. Editor: H.B. Sarnat. Grune and Stratton, London. Stanley, F.J. (1987): The changing face of cerebral palsy? Dev. Med. Child Neural., 29,258-270. Vojta, V. (1976): Die cerebralen bewegunsstorungen in Sanglingsalter. Enke, Stuttgard. Yamori, Y., Doi, S., Okuno, T., Mochixuki, Y ., Hojo, H. and Maruyama, P. (1978): Early diagnosis of cerebral motor disturbance. Brain Dev., 3, 139-140.
93
EHD 01095
Postural development in very low birth weight and normal birth weight infants Christopher Molteno=, Vivien Magasinera, Rauf Sayed” and Michael Karplusb *Departments of Paediatrics and Child Health and Community Health, University of Cape Town Cape Town and Red Cross War Memorial Children’s Hospital, Rondebosch (South Africa) and bDepartment of Pediatrics, Soroka Medical Centre, Ben-Gurion, University of Negev, Beer-Shelva (Israel) (Received 2 August 1988; revision received 19 June 1990, accepted 17 July 1990)
Summary In this study the seven postural responses selected by Vojta to evaluate neuromotor development were applied to 68 very low birth weight (VLBW) (> 1500 g) infants and to 28 healthy infants of normal birth weight (< 2500 g). Of the 68 VLBW infants, 41 were small for gestational age and 27 appropriate for gestational age. All infants were examined between 37 and 40 weeks postmenstrual age. They were all later assessed on the Griffiths Mental Developmental Scale at 12 and 18 months. There were significant differences in postural reactions between the two groups which confirmed the lower tone and greater extension previously described in very low birth weight infants. An important finding in the study was that poor head and trunk righting noted at four months corrected age in very low birth weight infants, was associated with less developed locomotion at 12 and 18 months as assessed by the Griffiths Mental Developmental Scale. Thus, a delay in maturation in very low birth weight infants which was apparent from the assessment of postural responses in early infancy was still identifiable on the locomotor subscales at 12 and 18 months. Five of Vojta’s responses were shown to be useful as part of the neurological assessment of high risk infants. postural responses; very low birth weight infants; locomotor development.
Correspondence to: Dr C.D. Molteno, University of South Florida, Department of Pediatrics, Box 15, 12901 Bruce B Downs Blvd., Tampa, Florida 33612-4799, U.S.A. 0378-3782/90/.$03.50 @ 1990 Elsevier Scientific Publishers Ireland Ltd. Published and Printed in Ireland
Introduction The improved quality of neonatal intensive care has greatly enhanced the chances of survival of infants who would otherwise have died. The survivors have, unfortunately, a higher risk of long term neurodevelopmental handicap. In Sweden [8] a decline in incidence of cerebral palsy was reported for the period 1954-1970, but from 1971-1978 it was found to have increased. More recently, Hagberg et al. [9] have reported a further rise in the incidence of cerebral palsy associated with a parallel decrease in perinatal mortality, especially in preterm infants. Stanley [ZO] has shown that there has been a marked fall in perinatal mortality in Western Australia with an increase in the rate of cerebral palsy among very low birth weight (VLBW) infants from 14.0/1000 live births in 1%8-1971 to 25.0/1000 in 1979-1981. In the first period (1968-1971) only 5.3% of all children with cerebral palsy had been less than 1500 g birth weight but this had risen to 11.5% in the years 1979-1981. In contrast, Haas et al. [7] reported an improved outcome in VLBW infants from 1977 to 1983. The incidence of neurological sequelae in their study declined from 9.2% in 1977-1979 to 3.7% in 1982-1983. The evaluation of neuromotor development is a valuable part of the neurological assessment of infants and this is particularly important in the follow up of all VLBW babies. It is known that the motor pattern of the VLBW infant differs from that of the full term, but existing tests do not serve to differentiate those babies who are neurologically normal in the longterm from those who are neurologically impaired. In 1976 Vojta [21] selected seven ‘postural reactions’ of normal, healthy infants in order to evaluate neuromotor development according to age. Deviations from the normal patterns could be considered as either ‘delayed’ or ‘pathological’. We felt that it would be useful to document the postural responses in VLBW infants. The aims of the study were (1) to investigate whether the motor patterns as determined by postural responses selected by Vojta differed between VLBW, AGA and SGA infants and controls at full term and follow-up and (2) to determine whether deviations detected by this examination technique would help in the early detection of cerebral palsy. Matprials and Methods Between August 1984 and June 1985, 68 VLBW (birth weight < 1500 g) and 28 healthy full term infants of normal birth weight (> 2500 g) were selected for study. The VLBW infants consisted of 41 smaIl for gestational age (SGA) (less than 10th centile using Lubchenco charts [l]) and 27 appropriate for gestational age (AGA) white and coloured (mixed ancestry) infants born in the Peninsula Maternal and Neonatal Service, which forms part of the University of Cape Town teaching hospitals. Gestational age was assessed by the method of Dubowitz et al. [3]. All infants, both VLBW and full term infants of normal birth weight (referred to as full term infants), were tested for postural reactions as specified by Vojta. Two VLBW and one full term infant were selected each week. If there were more than two VLBW infants available, those with the lowest birth weights and gestational
95 TABLE I Birthweight. gestational age, delivery and Apgar Scores in VLBW and full-term infants. Full-term
VLBW SGA
AGA
Number
41
21
28
Birthweight (g) S.D.
lux) 245
1299 118
3330 130
Gestational age (weeks) SD.
33.8 2.3
30.7 1.7
38.9 0.86
;:4%) 21
13 (48 qo) 14
28 (100%)
5.3 2.6 7.6 2.3
5.9 2.1 8.0 1.7
8.96 0.48 9.93 0.07
Delivery SVD Other Apgar Scores 1 min SD. 5min S.D.
‘SVD = spontaneous vertex delivery.
ages were enrolled in the study and examined between 37 and 40 weeks post menstrual age. The full term infants who were all examined on or after the second day of life (mean 3.7 days) were well grown, born by normal vertex deliveries, following normal pregnancies. They all established sustained respiration spontaneously after delivery and had unconplicated neonatal courses. Details of the infants are given in Table I. At the time of the first examination the mean weight of the VLBW infants was 1940 g, S.D. 240 and for the full term infants it was 3105 g, S.D. 534. The social backgrounds of all the infants were assessed on the ‘levels of living’ of Riley et al. [ 171, which are based on parental education and occupation and family income and housing density. This assessment has been compiled for the city of Cape Town using census data and yields scores of O-60, with the lower scores being most favourable. A pilot study involving 40 infants examined at term and four months was carried out prior to August 1984 and an evaluation chart was drawn up. All assessments were carried out by V.M.* in the nursery midway between feeds. A second identical evaluation of postural reactions was conducted at four months corrected age, i.e., 40 weeks post menstrual age plus 16 weeks (f 3 days). One *V.M. spent 3 weeks in the Department of Neonatology at Soroka Hospital, Beer Sheva, Israel under the supervision of M.K. V.M. became familiar with the evaluation of the postural responses and prepared a chart for recording the responses.
96
VLBW infant was not assessed at four months because of illness. At 12 and 18 months corrected age all infants were assessed by C.M. using the Griffiths Scales of Mental Development [2]. Assessment of postural reactions
(9
Traction response. With the infant supine, traction was applied to both arms until the trunk formed an angle of 45’ with the examination plane. The degree of head lag, arm flexion and position of the legs was noted.
(ii)
Landau response. The infant was held in a horizontal position with the examiner’s hand supporting the lower chest and upper abdomen. The position of the head, spinal curvature and degree of flexion of arms and legs was noted.
(iii)
Axillary hanging. The infant was held from behind, below the axillae and suspended vertically with the feet just clear of the table. Care was taken not to exert pressure on the back, which could have stimulated trunk extension. The position of the head and legs was noted.
(iv)
Side tilting according to Vojta. The infant was held vertically with the back to the examiner and tilted suddenly into the lateral horizontal position. The position of the head, trunk, upper arms and both legs was noted.
(v)
Collis horizontal suspension. With the infant lying on one side and the back to the examiner, the uppermost shoulder and hip joints were grasped, taking hold of the whole joint thus avoiding stretching the ligaments. The infant was then lifted just off the table. The positions of the head, trunk and free arm and leg were noted.
(vi)
Peiper response. The infant was placed supine with the head in the midline to prevent the influence of an ATNR. The examiner grasped the legs at the level of the knees, lifting the infant suddenly into inverted vertical suspension. The position of the head, trunk, arms and hands was noted.
(vii)
Collis vertical response. Following the Peiper response with the infant still in the vertical position, one leg was released and the position it took was noted. This leg was then grasped again and the same procedure was repeated with the other leg.
The behavioural state of the infant was recorded for each reaction. Four states were recognized - sleepy, awake with eyes open and minimal movement, awake and irritable or fussing and crying. All the results were recorded on a prescribed proforma and entered for computer analysis. The Chi-squared and the Fishers’ exact tests were used to test the differences between VLBW and full term infants for each of the postural reactions, and also the association between the assessment of pos-
97
tural reactions and locomotion. Student’s t-test.
Developmental quotients were compared using the
Results Postural responses and state at term The comparison of the postural reactions in the VLBW infants (corrected for prematurity) and the full term infants is shown in Table II. The VLBW infants tended to have lower tone and were more extended than the full term infants. On the traction response, the VLBW infants had significantly more head lag although many of the full term infants had more head lag than expected. One VLBW infant had a limp head drop which constitutes an abnormal response. The VLBW infants had less hip flexion, but there was no difference in arm flexion between the two groups. The Landau showed the VLBW infants to have more extension of head, trunk, arms and legs than the full term infants. On axillary hanging there was no difference in head posture, but the legs of the VLBW infants were more extended. The Vojta side tilting demonstrated more extension of the upper leg in the VLBW infants although there was no difference in head and trunk or arm posture. Similarly the Collis horizontal showed more extension of the VLBW infants’ legs only. There were no differences between the two groups on either the Peiper or the Collis vertical response. Regarding the state, the full term infants cried more during the Vojta (P < O.OOl),Collis horizontal (P< O.Ol), Peiper and Collis vertical (P< 0.001) response. Postural responses and state at four months At four months corrected age the VLBW still had more head lag than the full term infants on the traction response. They also had more arm extension and less hip flexion than the full term infants (Table II). There were no differences between the two groups on the Landau or the axillary hanging. The Vojta and Collis horizontal both showed the VLBW infants to have significantly less head and trunk righting responses than the full term infants. The two groups did not differ on the Peiper or Collis vertical reactions. There were no significant differences in state at four months. In both the term and four month assessments a number of full term infants had responses considered deviant by Vojta [19]. For example, at term 21.4% held their arms in suspension during the Landau and 17.9% had initial leg extension during axillary hanging. At four months a quarter still showed head lag and 42.8% arm extension on the traction response. These responses would have been more typical of VLBW infants. Comparison of AGA and SGA infants corrected to term andfour months There were no significant differences between SGA and AGA VLBW infants at 40 weeks post menstrual age. The SGA infants at four months corrected age had less head control on the traction response (P < 0.05) and cried more during the Vojta side tilting (P < 0.05) than the AGA infants.
58.8 41.2
Head flexed. trunk slightly curved P
%
Y/N
%
25.0
75.0
Head flexed, trunk curved
Elbow flex P
Elbow ext
Hip and knee in strong flex P
Qcl
G
Y-+/L
Hip and knee ext then flex or Hip in maximum abd. knee flex
Hip and knee in moderate flex
%
5.9
Moderate head lag
Full head control P
94.1
< 0.01
< 0.001
< 0.005
14.3
85.7
92.9
7.1
32.1
67.9
41.2
58.8
69.1
17.7
13.2
41.2
58.8
< 0.005
< 0.001
< 0.001
VLBW %
VLBW % Full-term %
4 months corrected age
0 months corrected age
Traction Marked head lag
Postural responses (significant results only).
TABLE II
78.6
21.4
loo.0
89.3
10.7
%
Full-term
99
E; d
V
9-9
Abbreviations: Flex, flexion; Ext, extension; Abd, abduction.
Hip and knee in ext then flex P
Hip and knee in loose flex
Righting of head, neck and trunk P
Collishorizontal Suspension of head, neck and trunk
TABLE II (continued)
25.0
58.8 < 0.01
75.0
41.2
67.6
32.4
< 0.005
VLBW %
VLBW %
Full-term %
4 months corrected age
0 months corrected age
100.0
Full-term 070
8
101 TABLE III Griffiths assessments at 12 and 18 months (mean f S.D.) Full-term n = 28
VLBW n = 68
106f
101 *
P value
I2 Months
Development quotient Sub-scale quotients Locomotion Personal/Social Hearing/speech Eye/hand Performance 18 Months Development quotient Sub-scale quotients Locomotion Personal/social Hearing/speech Eye/hand Performance
8
110 + 13 104* 5 103k 7 106* 7 108 + 10
1042
8
0.001
104f 13 101 f 8 101 + 11 101 f 7 98k 9
0.025 NS NS 0.003 0.001
6
992
8
0.002
104 + 10 101 + 6 104 f 10 103* 7 107+ 6
100 f 96 f 97 f 1002 102 f
13 10 12 8 10
0.015 0.015 NS 0.02
NS
Assessment at 12 and 18 months corrected age The VLBW infants performed less well on the Griffiths assessment at 12 and 18 months (Table III). Regarding the subtests, significant differences were found at 12 months in locomotion, eye-hand coordination and performance and at 18 months in personal/social, hearing and speech and performance. Three VLBW infants had neuro-developmental handicap (evidence of cerebral palsy and/or a DQ < 80). One had mild spastic diplegia and a normal DQ, a second spastic quadriplegia and a DQ of 65 and the third a DQ of 69 at 12 months. Cross correlation of the postural responses at term with DQs at 12 months revealed significances with arm extension bilaterally on the Landau response. There were no other significant associations between postural development and DQ at 12 or 18 months. However, associations were found between the locomotor subtests and postural responses. Extended arms on the Landau at 0 months corrected age in VLBW infants was associated with more advanced locomotor development at 12 months (P < 0.05). An open right hand in the Vojta side tilting at term corrected age was also associated with enhanced locomotion at both 12 and 18 months (P< 0.05). At four months corrected age delayed head and trunk righting on the left side in the Vojta side tilting was associated with a lower locomotor score at 12 and 18 months (P < 0.05). At four months corrected age delayed head and trunk righting on the right side in the Collis horizontal was associated with a lower locomotor score at 12 and 18 months (P < 0.05). Abduction of the shoulder with elbow flexion during the Peiper response was associated with more delayed locomotor development at 12 (P < 0.01) and 18 months (P < 0.03). The infants who cried more during the Landau, axillary hanging and Vojta at four
102
months corrected age performed less well on the locomotor subtest at 12 and 18 months (P < 0.05). Although all infants were drawn from the same hospital delivery population, the social backgrounds of the VLBW ‘infants (level of living scores, mean 35.6, SD. 26) were significantly less favourable than those of the full term infants (level of living scores, mean20, SD. 15.9; t = 3.88, P< 0.01). Discussion The assessment of postural reactions described by Vojta [21] was designed for the diagnosis of cerebral motor dysfunction. Noren and Franzen [14] tested 25 healthy infants from the newborn period to 18 months and found a considerable number of deviations from normal/optimal as specified by Vojta. The Vojta response yielded the highest number of deviations and the traction response the lowest, with the largest number noted at three months and the least in the newborn period. They did not specify the types of deviation. Hellstrom et al. [lo] found the traction response from 2 to 12 months frequently differed from that expected according to the description of Vojta, whereas the Landau and Collis vertical reactions followed, with a few exceptions, those expected for age. Japanese infants tested by Yumori et al. [22] were noted to have a tendency towards extensor reactions on the axillary hanging, Landau, Vojta, Collis horizontal and Collis vertical responses. Our full term infants also had a number of deviations from the expected responses, both at term and four months. Most of the deviations involved extension of the limbs which would have been more typical of the VLBW infants. The postural responses as specified by Vojta have not, to our knowledge, been applied to low birth weight infants. The first aim of the study was to compare the postural responses of VLBW, AGA and SGA infants and controls at full term and follow-up.There were significant differences in tone and degree of flexion between VLBW and full term infants. SaintAnne-Dargassies [18] found former premature infants to have less passive tone with wider angles and dangling of a larger amplitude than full term infants. The ex-premature infant also exhibited movements of greater amplitude and more varied, but they tended totire sooner. She put forward two possible explanations for the difference. Firstly, the full term infants had been more compressed in utero with their limbs being increasingly flexed in an elastic liquid milieu which was constantly dwindling and secondly, the ex-premature infants were generally less optimally nourished. The finding of lower tone and less flexion of VLBW infants also agrees with Palmer et al. [4] and with Howard et al. [l 11, who reported weaker responses especially on items involving muscle tone in premature infants. They were also more difficult to soothe. Forslund and Bjerre [5] found preterm infants to have lower muscle tone as judged by spontaneous posture of arms and legs, poor resistance to passive movements and slow arm recoil. In the traction test they had more head lag. Similarly, Kurtzberg et al. [12] reported lower tone in LBW infants, a higher incidence of crying following aversive items and a longer mean consolation latency. Our full term infants in contrast cried more during four of the seven responses. Brown [2] asso-
103
ciates motor development with sub-cortical brain maturation. He divides motor development into four stages, a first flexor and first extensor stage followed by a second flexor and extensor stage. The extension of the preterm infant could be associated with a prolonged secondary extensor developmental stage. Sarnat [I91has related the sequence of myelination to the changes in posture of the premature infant with advancing conceptional age. Prechtl and Nolte [I61 introduced a further variable, the differences in body weight which could affect muscle power. The VLBW infants in our study were still markedly underweight when compared to full term infants. The Griffiths Scales of Mental Development have been used by Goodman et al. [4] in VLBW follow up. At 12 months the locomotion subscales in both of their study groups (viz. ‘at risk’ and ‘normal’ VLBW infants) were higher than the other subscales. In our study the locomotion subscales in both VLBW and control groups were higher than other subscales at 12 but not at 18 months. The social disadvantage of the VLBW infants could have accounted for some of the developmental differences at follow-up. McCall [13], however, has postulated that mental development early in life, especially up until 18 to 24 months, is strongly canalized and slowly becomes less strongly canalized thereafter. Both genetic and environmental factors have minor correlations with mental performance before 18 to 24 months and both have increasing correlations after 24 months. Thus, although social class may have accounted for some of the differences in the personal/social and hearing/speech subtests at 18 months, social background is unlikely to have been responsible for the developmental differences at 12 months, which were on the locomotion, eye/hand and performance subtests. Regarding the second aim, to determine whether deviations detected by examining postural responses would help in the early detection of cerebral palsy, only two of the VLBW infants developed cerebral palsy - one a mild diplegia and the other a more severe spastic quadriplegia with general developmental delay. The child with diplegia showed no abnormal postures at term or at four months corrected age. The quadriplegic had no abnormal postures at term corrected age but unfortunately was ill at four months and was not examined. A greater number of cerebral palsied children would be needed to determine whether postural responses are useful in the early detection of cerebral palsy, but the limited findings of this study would not support it. The development of head and trunk righting distinguished VLBW from full term infants and also correlated with subsequent locomotor performance. The progress of head and trunk righting from birth to four months was particularly well demonstrated in the Vojta and Collis horizontal responses. Similarly, there was good correlation between head and trunk righting at four months on the Vojta and Collis horizontal responses and locomotion at both 12 and 18 months, suggesting a persisting maturational delay, although the locomotion subtest quotients for both the preterm and term infants were still within normal limits. Poor head and trunk righting is a strong indication of lack of trunk control which is a requirement for gross motor development. The statistical significance of the association between head and trunk righting and locomotor scores is important and warrants further attention.
104
In conclusion, the seven postural reactions selected by Vojta brought out significant differences between VLBW and full term infants at term corrected age. These differences related especially to lower tone and less flexion in VLBW infants. By four months the leg extension of the VLBW infants was no longer present, although delay in head and trunk control persisted. The head lag on the traction response was more marked in SGA than AGA infants. Head and trunk righting at four months was also related to locomotor development at 12 and 18 months as assessed by the Griffiths Scales of Mental Development. The postural responses are therefore useful in assessing aspects of VLBW infant development. Although this study was not helpful in detecting signs of later neurological abnormality, as a result of the study, a neurodevelopmental assessment chart was prepared. The chart combined the first five of Vojta’s postural responses together with an assessment of specific primitive reflexes and passive muscle tone. This chart is proving successful clinically and is being evaluated on a group of high risk VLBW infants with significant intraventricular haemorrhages. References 1 2 3 4
5 6 7
12
13
14 15
Battaglia, F. and Lubchenco, L. (1%7): A practical classification of newborn infants by weight for gestational age. J. Pediatr., 71, 159-163. Brown, J.K. (1974): General Neurology. In: Neonatal Medicine, p. 522. Editors: F. Cockburn and C. Drillien. Blackwell Scientific Publications, Edinburgh. Dubowitz, L.M.S., Dubowitz, V. and Goldberg C. (1970): Clinical assessment of gestational age in the newborninfant. J. Pediatr., 77, l-10. Goodman, M., Rothberg, A.D., Houston-McMilIan, J.E., Cooper, P.A., Cartwright, J.D. and Van der Velde, M.A. (1985): Effect of early neurodevelopmental therapy in normal and at-risk survivors of neonatal intensive care. Lancet, ii, 1327-1330. Forslund, M. and Bjerre, I. (1983): Neurological assessment of preterm infants at term conceptual age in comparison with normal full-term infants. Early Hum. Dev., 8, 195-208. Griffiths, R. (1976): The Abilities of Babies. A Study in Mental Measurement. Association for Research in Infant and Child Development, Amersham. Haas, G., Buchwald-Aal, M., Ledig, E. and Mentzel, H. (1986): Improved outcome in very low birth-weight infants from 1977-1983. Eur. J. Pediatr., 145,337-340. Hagberg, B., Hagberg, G. and Olow, I. (1984): The changing panorama of cerebral palsy - Sweden, 1959-1978. Acta Paediatr. Stand., 73,433-440. Hagberg, B., Hagberg, G., Olow, I. and von Wendt, L. (1989): The changing panorama of cerebral palsy in Sweden. V. The birth year period 1979-82. Acta Paediatr. Stand., 78,283-290. Hellstrom, B., Knutsson, E. and Wessman, A. (1982): The traction reaction in infancy - clinical and electromyographic study of normal infants. Neuropediatrics, 13,63-71. Howard, J., Parmelee, A.H., Kopp, C.B. and Littman, B.A. (1976): Neurologic comparison of preterm and full-term infants at term conceptional age. J. Pediatr., 88,995-1002. Kurtzburg, D.. Vaughan, H.G., Daum, C., Grellong, B.A., Albin, S. and Rotkin, L. (1979): Neurobehavioural performance of low birthweight infants at 40 weeks conceptional age: comparison with normal full-term infants. Dev. Med. Child Neurol., 21, 590-607. McCall, R. (1979): The Development of Intellectual Functioning in Infancy and the Prediction of Later IQ. In: Handbook of Infant Development, p. 732. Editor: J. Osofsky. John Wiley and Sons, New York. Noren, L. and Franzen, G. (1981): An evaluation of seven postural reactions (‘Lagereflexe’ selected by Vojta) in twenty five healthy infants. Neuropediatrics, 12, 308-312. Palmer, P.G., Dubowitz, L.M.S., Verghote, M. and Dubowitz, V. (1982): Neurological and neuro-
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behavioural differences between preterm infants at term and full-term newborn infants. Neuropediatrics, 13, 183-189. Prechtl, H.F. and Nolte. R. (1984): Motor behavior in preterm infants. In: Continuity of Neural Function from Prenatal to Postnatal Life. Clinics in Developmental Medicine, No. 94, p. 79. Editor: H.F.R. Prechtl, London S.I.M.P. with Blackwell Scientific, Philadelphia, Lippincott. Riley, N., Schuman. C., Romanowsky, P. and Gentle, R. (1984): Spatial Variations in the Levels of Living in the Cape Metropolitan Area. Second Inquiry into Poverty and Development in Southern Africa. Conference Paper No. 13, University of Cape Town, April. Saint-Anne Dargassies, S. (1977): Neurological Development in the Full-Term and Premature Neonate, pp. 222-224. Excerpta Medica, Amsterdam. Samat, H.B. (1984): Anatomic and Physiologic Correlates of Neurologic Development in Prematurity. In: Topics in Neonatal Neurology. Editor: H.B. Sarnat. Grune and Stratton, London. Stanley, F.J. (1987): The changing face of cerebral palsy? Dev. Med. Child Neural., 29,258-270. Vojta, V. (1976): Die cerebralen bewegunsstorungen in Sanglingsalter. Enke, Stuttgard. Yamori, Y., Doi, S., Okuno, T., Mochixuki, Y ., Hojo, H. and Maruyama, P. (1978): Early diagnosis of cerebral motor disturbance. Brain Dev., 3, 139-140.
