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Motor behavior of small for gestational age newborn infants
208
February, 1970 T h e ] o u r n a l o[ P E D I A T R I C S
Motor behavior of small for gestational age newborn infants Some aspects o[ motor behavior at term o[ small [or gestational age newborn in[ants and o[ normal [uU-term newborn in[ants were compared. Despite comparable conceptional ages o[ the two groups o[ in[ants, characteristic differences were [ound in some reflexes and automatic motor activities.
R. Michaelis, M.D., F. J. Schulte, M.D., and Renate Nolte, M.D. G(DTTINGEN~ GERMANY
T~E MATURATION of the central nervous system and the motor development of the newborn infant are more closely related to the actual conceptional age than to the age from birth or to birth weight. 1-5 Thus, the motor behavior of full-term small for gestational age infants is expected to be similar to that of newborn infants of normal weight at term. ~-7 A detailed study of reflexes and complex motor phenomena in small for gestational age versus normal weight newborn infants, both at term, revealed differences which are described in this paper.
SUBJECTS Two groups of newborn infants were examined. The gestational ages were calculated from the first day of the mother's last menstrual period and from the nerve-conduction velocityY~
From the Department o/Pediatrics, University o[ Ggttingen. This work was supported by grants [rom the Deutsche Forschungsgemeinscha#. RelJrlnt address: R. Mi~haelis, Kinderklinik der Universitaet GSttingen, 34 G6ttlngen, Humboldt-Alice 38, Germany Vol. 76, No. 2, pp. 208-2t3
Group I contained 22 small for gestational age newborn infants whose gestational ages ranged from 38 to 42 weeks. Birth weights were below the fifth percentile of the intrauterine growth curves according to Hosemann ~, 9 and well below the tenth percentile according to Lubchenco and associates? ~ The prenatal and perinatal histories are given in Table I. In all of the infants' serum, glucose and calcium as well as the hematocrits were checked during the first days of life until stabilization of these parameters occurred. Infants with severe hypoglycemia ( < 20 rag. per cent) and with a hematocrit of more than 65 per cent were treated with intravenous infusions of glucose solutions. The examination of infants with such postnatal complications was postponed until the infants' condition had stabilized. Group I I consisted of 25 normal weight newborn infants whose gestational ages ranged from 39 to 41 weeks. Birth weights were between the tenth and nintieth percentiles according to Hosemann s, 9 and above the tenth percentile according to Lubchenco and associates? ~ The pregnancies were in all ways uneventful and terminated
Volume 76 Number 2
Table
M o t o r behavior
209
I
No.
Gestational age (wk.)
Birth weight (Gm.)
1
39
2,270
2
40
2,360
Toxicosis
Vacuum extraction
3
39
2,080
Toxicosis
Twin
4
38
1,900
Twin
Hyperexcitability
5
38
1,900
Twin
Hyperexcitability
6
42
2,370
7
38
1,700
Toxicosis
8
39
2,120
Microplacenta
9
38
1,820
10
38
2,330
11
42
2,330
12
40
2,000
--
13
40
1,500
Microplacenta
14
40
2,270
--
15
38
2,250
--
16
40
1,750
Toxicosis
Hyperexcitability
17
41
2,130
Microplacenta
Hyperexcitability, hypertonia
18
38
2,300
--
Twin
Normal
19
38
2,120
--
Twin
Normal
20
40
2,300
--
Forceps
Normal
21
38
2,360
--
22
39
1,780
Microplacenta
Gestational history*
Postnatal findings');
Birth historyt Hct.:
B
65%
Normal Apathy
Hct.:
55%
Hyperexcitability
Hct. : 6 0 %
Normal
H c t . : 7 0 % ; glucose: 20 m g . / 1 0 0 ml. (2nd day)
Hyperexcitability, hypotonia
Hyperexcitability H c t . : 65 % ; glucose: 20 m g . / 1 0 0 ml. (3rd day)
--
Neurological findings in part A
Normal
m
Toxicosis
m
Hypotonia, hemisyndrome
Hct.:
62%
Hyperexcitability
Hct.:
63%
Normal
Glucose: 22 r a g . / 1 0 0 ml. ( l s t day)
Hyperexcltability
Normal Hct.: 55%
m
H c t . : 6 7 % glucose: 20 m g . / 1 0 0 ' ml. 1st day) ; 23 m g . / 100 ml. ( 2 n d day)
Normal
Normal Normal
"~Toxlcosis of mother means: maternal systolic blood pressure above 140 mm. Hg, edema, and albumlnuria, but no convulsions. tVacuum extraction in Infant No. 2: at the end of the birth, because of mother's high blood pressure. Infant well during labor and after birth. Forceps in Infant No. 20: at the end of the birth heart rate fell. Infant just after birth and later without any difficulties, no asphyxia. ++Hematocrit (ttct.) is indicated if higher than 55 per cent, serum glucose if lower than 25 mg. per 100 ml. For definition of hyperexcitahility, apathy, hypertonla, and hypotonia see Prechtl and Beintema.12
2 10
The ]ournal o/ Pediatrics February 1970
Michaelis, Schulte, and Nolte
spontaneously with normal deliveries9 No infant had postnatal complications. METHODS
All infants were examined between the third and seventh day after birth. The examination consisted of two parts. Part A was a routine pediatric examination which included a standard neurological examination. 11 The results of the neurological examination were summarized in the following neurological diagnoses, as defined by Prechtl and Beintema12: normal, hyperexcitability, apathy, hypertonia, or hypotonia of muscle tone. Discrepancies in syndromes between the two sides of the body were classified as hemisyndromes. Part B was a special neurological examination following immediately after part A, as defined below under Procedure and Scoring. Only infants who had no pathological findings in part A were included in group II. PROCEDURE
AND
SCORING
In part B the following reflexes and motor automatisms were evaluated : Moro response. A distinct and marked extension at the elbows, abduction of the arms, and opening of the hands in phase I, and a marked flexion at the elbows, adduction of the arms, and closing of the hands in phase I I were evaluated9 Scores. Phase I: absent, weak, or marked; phase I I : absent, weak, or marked. Asymmetric tonic neck reflex. This response is frequently absent in newborn infants at term. It can, however, be elicited more easily in the lower extremities. 12 Sometimes there is a quick extension of the lower extremity immediately followed by flexion. This pattern was coded as "weak." Scores9 Absent, weak, or marked ( > 2 seconds). Windmill motions of the arms. This pattern, frequently observed in preterm infants, exists only indistinctly in full-term infants. Scores. Marked: Marked extension at the elbows and opening of the hands when moving the arms forward. Marked flexion and closing of the hands when moving back;
weak: a similar pattern but poorly developed; absent. Head lifting in the prone position. As described by Preehtl and Beintema. 12 Scores. Absent; poor: short lifting once or twice; good: > 5 seconds. Rhythmic turning of the lifted head. Infant in the prone position. Scores. Good: head turning at least once to the right and to the left, .sustained head lifting; poor: turning without head lifting, or lifted head turned only once either to the right or to the left; absent. Standing response. The extension of hip and knee joints was evaluated when the infant was held in the upright position with the soles of the feet on the table. We did not study the "placing response." Scores. Good extension: marked extension at the hips and knees for more than 3 seconds; poor extension: occasional attempts; absent. Pattern of standing. Preterm infants tend to stand on the full sole, whereas infants at term prefer to stand on the lateral part of the sole. Scores. Mostly full sole; mostly lateral part of sole; both patterns. Stepping ~ovements. As described by Prechtl and Beintema. 12 Scores. Good response: more than two steps; poor response: 1 or 2 poor steps; absent. All infants of both groups were investigated while awake but not crying (states I I I or IV according to Prechtl and Beintema~2). The examination was done 1 ~ to 1 hour before feeding. No drugs had been given to the infants previously; in all cases hyperbilirubinemia was excluded. All infants were born in the head presentation. Differences in motor behavior between both groups of neonates were examined by frequency tables (4 cell and 6 cell) with the X2 test. For frequency tables with values of less than 5, a binomial test was applied9 RESULTS
The results are shown in Tables I I and I I I . There are significant differences in neonatal motor behavior between the groups.
Volume 76 Number 2
M o t o r behavior
2 11
of the arms are f r e q u e n t ; h e a d lifting in the prone position and rhythmic t u r n i n g of the lifted h e a d are i n f r eq u en t ; the standing response and stepping m o v e m e n t s are poor and p r e d o m i n a n t l y on full sole. Since the values of the frequency table were less t h a n 5 for the M o r o reflex phase I I and for r h y t h m i c a l t u r n i n g of the head, we checked w h e t h e r these differences still exist when calculated not only with the chi square test but according to the binomial distribution: M o r o reflex phase I I , p < 0.016 r h y t h m i c t u r n i n g of lifted head, p < 0.001. Both tests disclosed significant differences between the two groups of neonates in regard to these two m o t o r p h e n o m e n a . T h e question arises w h e t h e r the neurological abnormalities which were found in part A and surnmarized in T a b l e I could
As partly k n o wn from previous studies, ~, 12, ~a in ne wb o rn infants of n o r m a l birth weight the M o r o response consists of only short extension an d ab d u ct i o n followed by m a r k e d flexion an d ad d u ct i o n of the arms; the asymmetric tonic neck reflex is absent or unsustained; windmill motions of the arms are weak or absent; h e a d lifting in the prone position and r h y t h m i c t u r n in g of the h e a d are always present; a strong standing response on the lateral part of sole is predominant, and stepping m o v e m e n t s almost always occur. I n contrast, in small for gestational age ne w b o rn infants at term, the M o r o response often is characterized by a large extension a nd abduction of the arms, not always followed by phgse I I ; the asymmetric tonic neck reflex is sustained; windnfill motions
Table II
9
Scores
Group
Absent
Moro response I
S.f.g.a. ~ Normal
-2
Moro response II
S.f.g.a. Normal
--
S.f.g.a. Normal
Asymmetric tonic neck S.f.g.a. reflex Normal eS.f.g.a. = small for gestatlonaI age.
Motor patterns
Windmill motions of arms
I
Weak
I Marked
11 19
11 4
)r ~ 6.2; p < 0.02; df z 1
5
17 25
X2 = 6.35; p < 0.02; df z 1
10 17
1 7
11 1
X2 ~ 13.02; p < 0.001; df= 2
-4
3 16
19 5
X2 ~ 20.6; p ~ 0.001; dfz 1
--
--
Table III
Scores I Poor
Motor patterns
Group
Absent
Head lifting, prone position
S.f.g.a. ~ Normal
4 --
Rhythmic turning of lifted head
S.f.g.a. Normal
--
--
Standing response
S.f.g.a. Normal
--
19
S.f.g.a. Normal
14
Stepping movements
--
4
-1
Full sole Standing pattern
S.f.g.a. Normal ~S.f.g.a. = small for gestational age.
10
12 6
10
1
Good 8 25
X2 = 22.6; p ~ 0.001; df ~ 1
8 25
)c~ ~ 22.6; p ~ 0.001; df = 1
3
1
24
5
3 18
6
Lateral 8 6
X 2 ~
32;
df ~ 1
p
<
0.001; '~
)~2 = 21.9; p < 0.001; df = 2
Both 2 13
X2 z 10.53; p < 0.01; df'~ 2
2 12
Michaelis, Schulte, and Nolte
cause the differences in motor behavior between groups I and II. In this case, small for gestational age infants with neurological abnormalities found in part A would have significantly more findings in part B than small for gestationaI age infants without neurological abnormalities. To test this hypothesis for each infant in groups I and II, we counted how many of the following scores could be found: Moro response I, marked; Moro response II, weak or absent; asymmetric tonic neck reflex, marked; windmill motions, marked; head lifting in the prone position, poor or absent; rhythmic turning of the lifted head, absent; standing response, poor or absent; standing pattern, mostly full sole; stepping movements, poor or absent. The 22 infants in group I had an average of 5.4 findings (range 3 to 8; standard error (S.E.) = 0.26); the 25 infants in group I I had an average of 0.96 findings (range 0 to 4, S.E. = 0.24). The t test demonstrates a significant difference between the groups (t = 12.8; p < 0.001). The 11 infants in group I with neurological abnormalities found in part A had an average of 5.64 findings (S.E. = 0.37), the 11 infants without neurological abnormalities 5.27 (S.E . = 0.38). The t test demons trates no diffe rence ( t = 0.7, p < 0.4). DISCUSSION
The motor behavior of small for gestational age newborn infants is not dependent only on their gestational ages. The findings of Robinson ~ and some of our preliminary results suggest that some relatively simple reflex phenomena are closely related to the gestational age and are independent of birth weight. However, we found differences in the patterns of complex phenomena possibly more dependent on spinal integration and supraspinal control of motor neurons. Eleven small for gestational age infants were considered neurologically abnormal; the question arises as to whether or not the peculiarities of motor behavior in infants with intrauterine growth retardation are part of these abnormalities. This seems unlikely since the peculiar motor phenomena were found
The Journal o/ Pediatrics February 1970
equally often in both groups of small for gestational age infants, those who were considered to be neurologically normal as well as those diagnosed as abnormal. Furthermore, in part A the predominant abnormal finding was hyperexcitability, which can hardly explain the deviant motor phenomena in the small for gestational age group. In contrast to our results, Robinson 5 and Brett ~ found no differences in the motor behavior of small for gestational age newborn infants and normal weight ones. This might be caused by differences in scoring the findings or in the subjects. Whereas the cited authors evaluated the presence or absence of the examined reflexes, in our study the main interest was given to the quality of the elicited responses; therefore, we examined more complex motor phenomena. Recently, Graziani and associates 14 presented some investigations concerning neurological behavior in low-birth-weight newborn infants. They, too, found no differences related to gestational age. However, these investigators mainly examined reflexes with a low level of spinal or supraspinal control, which seemed to be more independent of disturbing influences, using them for the calculation of an average neuromaturational age. In contrast to Robinson, 5 Brett, 6 and Graziani and associates, ~4 we limited our examinations to mature infants with the the same gestational age but different birth weights. The differences we found between the two groups of newborn infants with the same gestational age might be in some way caused by chronic fetal distress (Gruenwald 1~) which could affect synaptic properties and conduction function in the central nervous system, as has been demonstrated in newborn animals. 16-~9 Further investigations are necessary to confirm such suppositions. SUMMARY
The motor behavior of small for gestational age infants at term and of normal weight full-term infants was compared. In contrast to full-term newborn infants of normal weight, small for gestational age infants
Volume 76 Number 2
more often have the following m o t o r patterns: M o r o response phase I marked, phase I I sometimes weak; marked asymmetric tonic neck reflex of the legs; frequent windmill motions of the arms; poor or absent head lifting a n d rhythmic t u r n i n g of the head in the prone position; poor or absent standing response" a n d stepping movements; standing p a t t e r n p r e d o m i n a n t l y full sole. REFERENCES 1. Gesell, A., and Amatruda, C. S.: The embryology of behavior, New York, 1945, Harper & Row, Publishers. 2. Hooker, D.: Early human fetal behavior with a preliminary note on double simultaneous fetal stimulation, Res. Publ. Ass. Res. Nerv. Ment. Dis. 33: 98, 1954. 3. Humphrey, T.: Some correlations between the appearance of human fetal reflexes and the development of the nervous system, Progr. Brain Res. 4: 93, 1964. 4. St. Anne Dargassies, S.: Neurological maturation of the premature infant of 28 to 41 weeks gestational age, in Falkner, F., editor: Human development, Philadelphia, 1966, W. B. Saunders Co. 5. Robinson, R. J.: Assessment of gestational age by neurological examination, Arch. Dis. Child. 41: 437, 1966. 6. Brett, E.: The estimation of foetal maturity by the neurological examination of the neonate, in Gestational age, size, and maturity, Spastics Society, London, 1965, Heinemann Medical Publishers, Ltd. 7. Minkowski, A.: Development of the nervous system in early life, in Falkner, F., editor: Human development, Philadelphia, 1966, W. B. Saunders Co. 8. Hosemann, H.: "Schwangerschaftsdauer und Neugeborenengewicht, Arch. Gynaek. 176: 109, 1948.
M o t o r behavior
2 13
9. Gruenwald, P.: Growth of the human fetus. I. Normal growth and its variation, Amer. J. Obstet. Gynec. 94: 1112, 1966. 10. Lubchenco, L. O., Hansman, C., Dressier, M., and Boyd, E.: Intrauterine growth estimated from liveborn, birth weight data at 24 to 42 weeks of gestation, Pediatrics 32: 793, 1963. 11. Joppich, G., and Schulte, F. J.: Neurologie des Neugeborenen, Berlin, 1968, SpringerVerlag. 12. Prechtl, H. F. R., and Belntema, D.: The neurological examination of the newborn, London, 1964, Heinemann Medical Books, Ltd. 13. Babson, S. G., and McKinnon, C. M.: Determination of gestational age in premature infants, Lancet 1: 7, 1967. 14. Graziani, L. T., Weitzman, E. D., and Velasco, M. S. A.: Neurologic maturation and auditory evoked responses in low birth weight infants, Pediatrics 41: 483, 1968. 15. Gruenwald, P.: Chronic fetal distress and placental insufficiency, Biol. Neonat. 5: 215, 1963. 16. Benton, J. W., Moser, H. W., Dodge, P. R., and Cart, S.: Modification of the schedule of myelination in the rat by early nutritional deprivation, Pediatrics 38: 801, 1966. 17. Chase, H. P., Dorsey, J., and McKhann, G. M.: The effect of malnutrition on the synthesis of a myelin lipid, Pediatrics 40: 551, 1967. 18. Dobbing, J.: The effect of undernutrition on myelination in the central nervous system, Biol. Neonat. 9: 132, 1966. 19. Dravid, A. R., and Himwlch, W. A.: Biochemical studies of the central nervous system of the dog during maturation, Progr. Brain Res. 9: 170, 1964. 20. Schulte, J. F., Michaelis, R., Linke, I., and Nolte, R.: Motor nerve conduction velocity in term, preterm, and small-for-dates newborn infants, Pediatrics 42: 17, 1968.
February, 1970 T h e ] o u r n a l o[ P E D I A T R I C S
Motor behavior of small for gestational age newborn infants Some aspects o[ motor behavior at term o[ small [or gestational age newborn in[ants and o[ normal [uU-term newborn in[ants were compared. Despite comparable conceptional ages o[ the two groups o[ in[ants, characteristic differences were [ound in some reflexes and automatic motor activities.
R. Michaelis, M.D., F. J. Schulte, M.D., and Renate Nolte, M.D. G(DTTINGEN~ GERMANY
T~E MATURATION of the central nervous system and the motor development of the newborn infant are more closely related to the actual conceptional age than to the age from birth or to birth weight. 1-5 Thus, the motor behavior of full-term small for gestational age infants is expected to be similar to that of newborn infants of normal weight at term. ~-7 A detailed study of reflexes and complex motor phenomena in small for gestational age versus normal weight newborn infants, both at term, revealed differences which are described in this paper.
SUBJECTS Two groups of newborn infants were examined. The gestational ages were calculated from the first day of the mother's last menstrual period and from the nerve-conduction velocityY~
From the Department o/Pediatrics, University o[ Ggttingen. This work was supported by grants [rom the Deutsche Forschungsgemeinscha#. RelJrlnt address: R. Mi~haelis, Kinderklinik der Universitaet GSttingen, 34 G6ttlngen, Humboldt-Alice 38, Germany Vol. 76, No. 2, pp. 208-2t3
Group I contained 22 small for gestational age newborn infants whose gestational ages ranged from 38 to 42 weeks. Birth weights were below the fifth percentile of the intrauterine growth curves according to Hosemann ~, 9 and well below the tenth percentile according to Lubchenco and associates? ~ The prenatal and perinatal histories are given in Table I. In all of the infants' serum, glucose and calcium as well as the hematocrits were checked during the first days of life until stabilization of these parameters occurred. Infants with severe hypoglycemia ( < 20 rag. per cent) and with a hematocrit of more than 65 per cent were treated with intravenous infusions of glucose solutions. The examination of infants with such postnatal complications was postponed until the infants' condition had stabilized. Group I I consisted of 25 normal weight newborn infants whose gestational ages ranged from 39 to 41 weeks. Birth weights were between the tenth and nintieth percentiles according to Hosemann s, 9 and above the tenth percentile according to Lubchenco and associates? ~ The pregnancies were in all ways uneventful and terminated
Volume 76 Number 2
Table
M o t o r behavior
209
I
No.
Gestational age (wk.)
Birth weight (Gm.)
1
39
2,270
2
40
2,360
Toxicosis
Vacuum extraction
3
39
2,080
Toxicosis
Twin
4
38
1,900
Twin
Hyperexcitability
5
38
1,900
Twin
Hyperexcitability
6
42
2,370
7
38
1,700
Toxicosis
8
39
2,120
Microplacenta
9
38
1,820
10
38
2,330
11
42
2,330
12
40
2,000
--
13
40
1,500
Microplacenta
14
40
2,270
--
15
38
2,250
--
16
40
1,750
Toxicosis
Hyperexcitability
17
41
2,130
Microplacenta
Hyperexcitability, hypertonia
18
38
2,300
--
Twin
Normal
19
38
2,120
--
Twin
Normal
20
40
2,300
--
Forceps
Normal
21
38
2,360
--
22
39
1,780
Microplacenta
Gestational history*
Postnatal findings');
Birth historyt Hct.:
B
65%
Normal Apathy
Hct.:
55%
Hyperexcitability
Hct. : 6 0 %
Normal
H c t . : 7 0 % ; glucose: 20 m g . / 1 0 0 ml. (2nd day)
Hyperexcitability, hypotonia
Hyperexcitability H c t . : 65 % ; glucose: 20 m g . / 1 0 0 ml. (3rd day)
--
Neurological findings in part A
Normal
m
Toxicosis
m
Hypotonia, hemisyndrome
Hct.:
62%
Hyperexcitability
Hct.:
63%
Normal
Glucose: 22 r a g . / 1 0 0 ml. ( l s t day)
Hyperexcltability
Normal Hct.: 55%
m
H c t . : 6 7 % glucose: 20 m g . / 1 0 0 ' ml. 1st day) ; 23 m g . / 100 ml. ( 2 n d day)
Normal
Normal Normal
"~Toxlcosis of mother means: maternal systolic blood pressure above 140 mm. Hg, edema, and albumlnuria, but no convulsions. tVacuum extraction in Infant No. 2: at the end of the birth, because of mother's high blood pressure. Infant well during labor and after birth. Forceps in Infant No. 20: at the end of the birth heart rate fell. Infant just after birth and later without any difficulties, no asphyxia. ++Hematocrit (ttct.) is indicated if higher than 55 per cent, serum glucose if lower than 25 mg. per 100 ml. For definition of hyperexcitahility, apathy, hypertonla, and hypotonia see Prechtl and Beintema.12
2 10
The ]ournal o/ Pediatrics February 1970
Michaelis, Schulte, and Nolte
spontaneously with normal deliveries9 No infant had postnatal complications. METHODS
All infants were examined between the third and seventh day after birth. The examination consisted of two parts. Part A was a routine pediatric examination which included a standard neurological examination. 11 The results of the neurological examination were summarized in the following neurological diagnoses, as defined by Prechtl and Beintema12: normal, hyperexcitability, apathy, hypertonia, or hypotonia of muscle tone. Discrepancies in syndromes between the two sides of the body were classified as hemisyndromes. Part B was a special neurological examination following immediately after part A, as defined below under Procedure and Scoring. Only infants who had no pathological findings in part A were included in group II. PROCEDURE
AND
SCORING
In part B the following reflexes and motor automatisms were evaluated : Moro response. A distinct and marked extension at the elbows, abduction of the arms, and opening of the hands in phase I, and a marked flexion at the elbows, adduction of the arms, and closing of the hands in phase I I were evaluated9 Scores. Phase I: absent, weak, or marked; phase I I : absent, weak, or marked. Asymmetric tonic neck reflex. This response is frequently absent in newborn infants at term. It can, however, be elicited more easily in the lower extremities. 12 Sometimes there is a quick extension of the lower extremity immediately followed by flexion. This pattern was coded as "weak." Scores9 Absent, weak, or marked ( > 2 seconds). Windmill motions of the arms. This pattern, frequently observed in preterm infants, exists only indistinctly in full-term infants. Scores. Marked: Marked extension at the elbows and opening of the hands when moving the arms forward. Marked flexion and closing of the hands when moving back;
weak: a similar pattern but poorly developed; absent. Head lifting in the prone position. As described by Preehtl and Beintema. 12 Scores. Absent; poor: short lifting once or twice; good: > 5 seconds. Rhythmic turning of the lifted head. Infant in the prone position. Scores. Good: head turning at least once to the right and to the left, .sustained head lifting; poor: turning without head lifting, or lifted head turned only once either to the right or to the left; absent. Standing response. The extension of hip and knee joints was evaluated when the infant was held in the upright position with the soles of the feet on the table. We did not study the "placing response." Scores. Good extension: marked extension at the hips and knees for more than 3 seconds; poor extension: occasional attempts; absent. Pattern of standing. Preterm infants tend to stand on the full sole, whereas infants at term prefer to stand on the lateral part of the sole. Scores. Mostly full sole; mostly lateral part of sole; both patterns. Stepping ~ovements. As described by Prechtl and Beintema. 12 Scores. Good response: more than two steps; poor response: 1 or 2 poor steps; absent. All infants of both groups were investigated while awake but not crying (states I I I or IV according to Prechtl and Beintema~2). The examination was done 1 ~ to 1 hour before feeding. No drugs had been given to the infants previously; in all cases hyperbilirubinemia was excluded. All infants were born in the head presentation. Differences in motor behavior between both groups of neonates were examined by frequency tables (4 cell and 6 cell) with the X2 test. For frequency tables with values of less than 5, a binomial test was applied9 RESULTS
The results are shown in Tables I I and I I I . There are significant differences in neonatal motor behavior between the groups.
Volume 76 Number 2
M o t o r behavior
2 11
of the arms are f r e q u e n t ; h e a d lifting in the prone position and rhythmic t u r n i n g of the lifted h e a d are i n f r eq u en t ; the standing response and stepping m o v e m e n t s are poor and p r e d o m i n a n t l y on full sole. Since the values of the frequency table were less t h a n 5 for the M o r o reflex phase I I and for r h y t h m i c a l t u r n i n g of the head, we checked w h e t h e r these differences still exist when calculated not only with the chi square test but according to the binomial distribution: M o r o reflex phase I I , p < 0.016 r h y t h m i c t u r n i n g of lifted head, p < 0.001. Both tests disclosed significant differences between the two groups of neonates in regard to these two m o t o r p h e n o m e n a . T h e question arises w h e t h e r the neurological abnormalities which were found in part A and surnmarized in T a b l e I could
As partly k n o wn from previous studies, ~, 12, ~a in ne wb o rn infants of n o r m a l birth weight the M o r o response consists of only short extension an d ab d u ct i o n followed by m a r k e d flexion an d ad d u ct i o n of the arms; the asymmetric tonic neck reflex is absent or unsustained; windmill motions of the arms are weak or absent; h e a d lifting in the prone position and r h y t h m i c t u r n in g of the h e a d are always present; a strong standing response on the lateral part of sole is predominant, and stepping m o v e m e n t s almost always occur. I n contrast, in small for gestational age ne w b o rn infants at term, the M o r o response often is characterized by a large extension a nd abduction of the arms, not always followed by phgse I I ; the asymmetric tonic neck reflex is sustained; windnfill motions
Table II
9
Scores
Group
Absent
Moro response I
S.f.g.a. ~ Normal
-2
Moro response II
S.f.g.a. Normal
--
S.f.g.a. Normal
Asymmetric tonic neck S.f.g.a. reflex Normal eS.f.g.a. = small for gestatlonaI age.
Motor patterns
Windmill motions of arms
I
Weak
I Marked
11 19
11 4
)r ~ 6.2; p < 0.02; df z 1
5
17 25
X2 = 6.35; p < 0.02; df z 1
10 17
1 7
11 1
X2 ~ 13.02; p < 0.001; df= 2
-4
3 16
19 5
X2 ~ 20.6; p ~ 0.001; dfz 1
--
--
Table III
Scores I Poor
Motor patterns
Group
Absent
Head lifting, prone position
S.f.g.a. ~ Normal
4 --
Rhythmic turning of lifted head
S.f.g.a. Normal
--
--
Standing response
S.f.g.a. Normal
--
19
S.f.g.a. Normal
14
Stepping movements
--
4
-1
Full sole Standing pattern
S.f.g.a. Normal ~S.f.g.a. = small for gestational age.
10
12 6
10
1
Good 8 25
X2 = 22.6; p ~ 0.001; df ~ 1
8 25
)c~ ~ 22.6; p ~ 0.001; df = 1
3
1
24
5
3 18
6
Lateral 8 6
X 2 ~
32;
df ~ 1
p
<
0.001; '~
)~2 = 21.9; p < 0.001; df = 2
Both 2 13
X2 z 10.53; p < 0.01; df'~ 2
2 12
Michaelis, Schulte, and Nolte
cause the differences in motor behavior between groups I and II. In this case, small for gestational age infants with neurological abnormalities found in part A would have significantly more findings in part B than small for gestationaI age infants without neurological abnormalities. To test this hypothesis for each infant in groups I and II, we counted how many of the following scores could be found: Moro response I, marked; Moro response II, weak or absent; asymmetric tonic neck reflex, marked; windmill motions, marked; head lifting in the prone position, poor or absent; rhythmic turning of the lifted head, absent; standing response, poor or absent; standing pattern, mostly full sole; stepping movements, poor or absent. The 22 infants in group I had an average of 5.4 findings (range 3 to 8; standard error (S.E.) = 0.26); the 25 infants in group I I had an average of 0.96 findings (range 0 to 4, S.E. = 0.24). The t test demonstrates a significant difference between the groups (t = 12.8; p < 0.001). The 11 infants in group I with neurological abnormalities found in part A had an average of 5.64 findings (S.E. = 0.37), the 11 infants without neurological abnormalities 5.27 (S.E . = 0.38). The t test demons trates no diffe rence ( t = 0.7, p < 0.4). DISCUSSION
The motor behavior of small for gestational age newborn infants is not dependent only on their gestational ages. The findings of Robinson ~ and some of our preliminary results suggest that some relatively simple reflex phenomena are closely related to the gestational age and are independent of birth weight. However, we found differences in the patterns of complex phenomena possibly more dependent on spinal integration and supraspinal control of motor neurons. Eleven small for gestational age infants were considered neurologically abnormal; the question arises as to whether or not the peculiarities of motor behavior in infants with intrauterine growth retardation are part of these abnormalities. This seems unlikely since the peculiar motor phenomena were found
The Journal o/ Pediatrics February 1970
equally often in both groups of small for gestational age infants, those who were considered to be neurologically normal as well as those diagnosed as abnormal. Furthermore, in part A the predominant abnormal finding was hyperexcitability, which can hardly explain the deviant motor phenomena in the small for gestational age group. In contrast to our results, Robinson 5 and Brett ~ found no differences in the motor behavior of small for gestational age newborn infants and normal weight ones. This might be caused by differences in scoring the findings or in the subjects. Whereas the cited authors evaluated the presence or absence of the examined reflexes, in our study the main interest was given to the quality of the elicited responses; therefore, we examined more complex motor phenomena. Recently, Graziani and associates 14 presented some investigations concerning neurological behavior in low-birth-weight newborn infants. They, too, found no differences related to gestational age. However, these investigators mainly examined reflexes with a low level of spinal or supraspinal control, which seemed to be more independent of disturbing influences, using them for the calculation of an average neuromaturational age. In contrast to Robinson, 5 Brett, 6 and Graziani and associates, ~4 we limited our examinations to mature infants with the the same gestational age but different birth weights. The differences we found between the two groups of newborn infants with the same gestational age might be in some way caused by chronic fetal distress (Gruenwald 1~) which could affect synaptic properties and conduction function in the central nervous system, as has been demonstrated in newborn animals. 16-~9 Further investigations are necessary to confirm such suppositions. SUMMARY
The motor behavior of small for gestational age infants at term and of normal weight full-term infants was compared. In contrast to full-term newborn infants of normal weight, small for gestational age infants
Volume 76 Number 2
more often have the following m o t o r patterns: M o r o response phase I marked, phase I I sometimes weak; marked asymmetric tonic neck reflex of the legs; frequent windmill motions of the arms; poor or absent head lifting a n d rhythmic t u r n i n g of the head in the prone position; poor or absent standing response" a n d stepping movements; standing p a t t e r n p r e d o m i n a n t l y full sole. REFERENCES 1. Gesell, A., and Amatruda, C. S.: The embryology of behavior, New York, 1945, Harper & Row, Publishers. 2. Hooker, D.: Early human fetal behavior with a preliminary note on double simultaneous fetal stimulation, Res. Publ. Ass. Res. Nerv. Ment. Dis. 33: 98, 1954. 3. Humphrey, T.: Some correlations between the appearance of human fetal reflexes and the development of the nervous system, Progr. Brain Res. 4: 93, 1964. 4. St. Anne Dargassies, S.: Neurological maturation of the premature infant of 28 to 41 weeks gestational age, in Falkner, F., editor: Human development, Philadelphia, 1966, W. B. Saunders Co. 5. Robinson, R. J.: Assessment of gestational age by neurological examination, Arch. Dis. Child. 41: 437, 1966. 6. Brett, E.: The estimation of foetal maturity by the neurological examination of the neonate, in Gestational age, size, and maturity, Spastics Society, London, 1965, Heinemann Medical Publishers, Ltd. 7. Minkowski, A.: Development of the nervous system in early life, in Falkner, F., editor: Human development, Philadelphia, 1966, W. B. Saunders Co. 8. Hosemann, H.: "Schwangerschaftsdauer und Neugeborenengewicht, Arch. Gynaek. 176: 109, 1948.
M o t o r behavior
2 13
9. Gruenwald, P.: Growth of the human fetus. I. Normal growth and its variation, Amer. J. Obstet. Gynec. 94: 1112, 1966. 10. Lubchenco, L. O., Hansman, C., Dressier, M., and Boyd, E.: Intrauterine growth estimated from liveborn, birth weight data at 24 to 42 weeks of gestation, Pediatrics 32: 793, 1963. 11. Joppich, G., and Schulte, F. J.: Neurologie des Neugeborenen, Berlin, 1968, SpringerVerlag. 12. Prechtl, H. F. R., and Belntema, D.: The neurological examination of the newborn, London, 1964, Heinemann Medical Books, Ltd. 13. Babson, S. G., and McKinnon, C. M.: Determination of gestational age in premature infants, Lancet 1: 7, 1967. 14. Graziani, L. T., Weitzman, E. D., and Velasco, M. S. A.: Neurologic maturation and auditory evoked responses in low birth weight infants, Pediatrics 41: 483, 1968. 15. Gruenwald, P.: Chronic fetal distress and placental insufficiency, Biol. Neonat. 5: 215, 1963. 16. Benton, J. W., Moser, H. W., Dodge, P. R., and Cart, S.: Modification of the schedule of myelination in the rat by early nutritional deprivation, Pediatrics 38: 801, 1966. 17. Chase, H. P., Dorsey, J., and McKhann, G. M.: The effect of malnutrition on the synthesis of a myelin lipid, Pediatrics 40: 551, 1967. 18. Dobbing, J.: The effect of undernutrition on myelination in the central nervous system, Biol. Neonat. 9: 132, 1966. 19. Dravid, A. R., and Himwlch, W. A.: Biochemical studies of the central nervous system of the dog during maturation, Progr. Brain Res. 9: 170, 1964. 20. Schulte, J. F., Michaelis, R., Linke, I., and Nolte, R.: Motor nerve conduction velocity in term, preterm, and small-for-dates newborn infants, Pediatrics 42: 17, 1968.