Five Early Milestones in Premature Infants Max Sugar, MD Louisiana State University School o f Medicine
The onset of five early milestones was studied in premature and full-term infants. The milestones are: recognition of mother's voice and face, 3month smile, following through 180 ~ and two hand-eye coordination. It was hypothesized that premature infants would show delay in acquiring milestones related to time separated from mother. Compared to full-term infants, the prematures had a significant difference in the means only for the onset of smiling, and no effect related to maternal separation.
ABSTRACT:
Reported comparisons of premature and full-term infants have been based on psychological and educational achievements involving extensive testing. No age is given for the appearance of developmental milestones in premature infants, except to add a correction factor based on gestational age [ 1 : 2 5 5 ] . A clinical guideline of expectations for premature infants' milestones that may be observed easily might be useful in assessing some aspects of the premature infant's development. This paper, part of a longitudinal study of milestones in prematures in the first 2 years of life, reports on five such milestones in the first 6 months postdelivery. These are the onset age of 3-month smiling, following, t w o hand-eye coordination, recognition of mother's voice, and recognition of mother's face. It was hypothesized that since prematures may be separated from Dr. Sugar is Clinical Professor of Psychiatry, Louisiana State University School of Medicine, New Orleans, Louisiana. Address reprint requests to Dr. Sugar, 17 Rosa Park, New Orleans, Louisiana 70115. The author is grateful to Juan-Washington, MD, former Director, and his staff, of the Newborn Intensive Care Unit, and to the Premature Outpatient Clinic of Charity Hospital in New Orleans for their excellent cooperation during this study; M. Kelly, RN, former Director, and her staff, at the Mary Buck City Health Clinic; Lawrence Van Egeren, PhD, and Lawrence Weber, PhD, for help with the statistics; David Taylor for the computer programming; David A. Freedman, MD, and Gerald Wiener, PhD, for their critical reading of the manuscript. Child Psychiatry and Human Development
Vol. 8(1), Fall 1977
11
12
Child Psychiatry and Human Development
t h e i r m o t h e r s f o r several m o n t h s , t h e y w o u l d s h o w delay in acquiring d e v e l o p m e n t a l m i l e s t o n e s r e l e a t e d t o t i m e o f s e p a r a t i o n f r o m the m o t h e r . T w o o f t h e m i l e s t o n e s - - r e c o g n i t i o n o f m o t h e r ' s voice a n d f a c e - - a r e t h e o r i z e d t o be i n t i m a t e l y involved in t h e a t t a c h m e n t p r o c ess a n d require t h e m o t h e r ' s p r e s e n c e f o r their d e v e l o p m e n t . F o r the d e v e l o p m e n t o f the o t h e r t h r e e m i l e s t o n e s - - 3 - m o n t h smile, following, a n d t w o h a n d - e y e c o o r d i n a t i o n - - i t is felt t h a t t h e regular and c o n s t a n t p r e s e n c e o f a significant p a r e n t i n g figure is n o t n e e d e d . A c o m p a r i s o n o f o n s e t ages in t h e s e t w o g r o u p s with t h e i r d i s p a r a t e relation to the a t t a c h m e n t p r o c e s s m i g h t d i f f e r e n t i a t e the e f f e c t s o f m a t e r n a l s e p a r a t i o n due to a l e n g t h y n u r s e r y stay f r o m biological c o n t r i b u t i o n s to t h e d e v e l o p m e n t o f these m i l e s t o n e s . E a c h o f these i t e m s t h u s has i m p o r t a n c e as an a c h i e v e m e n t b y the i n f a n t a n d as a s t i m u l u s to the m o t h e r in her p l e a s u r a b l e i n v o l v e m e n t with t h e i n f a n t a n d its d e v e l o p m e n t .
Method After the first months, some pediatricians may calculate the onset of all milestones by estimated gestational age (EGA) for low birth weight infants, but my impression is that generally they use birth weight for expectations of development for all infants. Thus, the focal point here is the birth weight, since this was recorded regularly and determined the prematures' discharge from the Newborn Intensive Care Unit. Since the gestational age was irregularly noted on the charts and its accuracy questionable, while the birth weight and length were routinely recorded, the definition of prematurity used here is a birth weight of 2,500 gm or less with a birth length of 47 cm or less (heel to crown) and (whenever noted) an EGA of 37 weeks or less [2:99]. In this paper, for brevity, birth weight of < 2,500 gm will also refer to birth length of < 47 cm. The infants were divided into groups by birth weight, EGA, and nursery stay as follows: (a) birth weight--as prematures of < 1,250 gm with < 47 cm length; > 1,250 gm but < 2,500 gin, with < 47 cm length; and a full-term group > 2,500 gm with > 47 cm length; (b) EGA--as < 32 weeks' gestation, < 37 weeks' gestation, and ~ 38 weeks' gestation; and (c) length of nursery stay--as > 7 weeks, 3 to 7 weeks, and < 2 weeks. Onset age for the milestones here is the chronological age after birth for all the infants. This allows the postdelivery onset age of the milestones to be determined in prematures and full-terms and for the two groups to be compared. A coeval determination is possible of the effects, if any, of maternal separation from the infant on the development of the milestones. In this study, the infants were born between 1969 and 1975. The mothers of the premature and full-term infants were separated from them and uninvolved in their care until discharge from the municipal hospital. Premature infants were discharged from the N.I.C.U. when stabilized and weighing about 41/~pounds.
Max Sugar
13
TABLE I SCORING OF THE MILESTONES
Milestones
Average Onset Age (Range is 2 months)a
Upper Age I Limit f o r Inclusion b
Stimuli Used
Presence, Duration and/or Confirmation of Milestone
3-Months Smile (3,4)
3 months
20 weeks Observer' s, other's Present for or mother's voice, l second and face (with mouth repeatable.c, d open or smiling or moving), face-mask, l i g h t or bell.
Following (3)
4 months
24 weeks Any slowly moving object in visual field.
Follows slowlymoving object with head and eyes through arc of 180v and repeatable, d
2 Hand-Eye Coordination (51
7 months
38 weeks Any object that is i n v i t i n g and capable of being grasped with 2 hands.
Grasping with 2 hands in response to visual stimulus and repeatable~,d
Recognition of Mother's Voice (6)
12 weeks
20 weeks
Mother's or mothering person's voice with face out of view.
Recognition of Mother's Face (7)
12 weeks
20 Mother's face weeks without speech.
Smiling, being soothed, discontinued crying or recognition response only to mother's voice and repeatable,c Smiling, being soothed, discontinued crying or recognition response only to mother's face and
repeatable, c
aAs derived from l i t e r a t u r e cited in the l e f t hand column. bIf not present at exam before upper age l i m i t , but had monthly exams therea f t e r , then scored as of date observed; otherwise, scored as "no data" for that milestone for the infant. CBased on mother's history i f confirmed on exam within l month of her date. dBased on exam i f seen at least once before upper age and then monthly.
14
Child Psychiatry and Human Development
The infants in this study were seen in the premature clinic of the local municipal hospital or at a city health clinic. Beginning 2 weeks after hospital discharge, the premature infants routinely came to the premature clinic monthly until 6 months of age, then bimonthly until age I year, then semiannually until 3 years of age, and annually thereafter. Full-term infants and a few prematures were observed at the neighborhood city health clinic, which offered routine well-baby examinations for all newborns in the area beginning at 4 days, then on a monthly basis for the first year, then every 3 months for the second year. Socioeconomically, the city health clinic had a population similar to that of the municipal hospital, and most o f the infants were delivered at this hospital. The premature and full-term groups were similar in both clinics socioeconomically and racially, with 91% of both groups of lower socioeconomic status (note that lower S.E.S. conforms to the definition for classes 4 and 5 of Hollingshead and Redlich [3] ) and 9% middle S.E.S. made up of 90% black and 10% white infants. Criteria for scoring each milestone are listed in Table I [ 4 - 8 ] . The total population consisted of 535 infants divided by birth weight and as follows: 349 p r e m a t u r e s - 136 prematures weighing 1,250 gm or less (mean 1,036, S.D. 159) and 213 prematures weighing ove~ 1,250 gm (mean 1751, S.D. 345); 186 full-term infants weighing over 2,500 gm (mean 3,282, S.D. 454). There were many drop-outs and infants' visits often did not meet the criteria for time limits indicated above. Thus, the numbers reported on for each milestone noted in the tables differ somewhat, but they meet the requirements listed in Table I, and there are about 50 for each milestone in each weight group. Among the total o f 535 infants, there were 49 from multiple births from different weight categories as follows: 17 in the lower-weight prematures, 29 in the upper-weight prematures, and 3 in the full-term group. In some multiple births, the twinship had been lost through death at birth or neonatally as follows by weight: < 1,250 gm --13 infants; > 1,250 gin--none; full-term--3 infants. The mean gestational age for the smaller prematures--< 1,250 gm (136) of whom 112 had EGA recorded-was 29 weeks (S.D. 2.9); for the large prematures--> 1,250 gm (213) of whom 160 had EGA recorded--was 34 weeks (S.D. 3.1); and for the 186 full-terms--> > 2,500 gin, EGA recorded--was 40 weeks (S.D. 0.0). These figures are an indication of poor recording for EGA. (There were 13 infants diagnosed as small for gestational age; 6 were < 1,250 gm with EGA range 28 to 40 weeks, and 7 were > 1,250 gm with EGA range of 30 to 40 weeks. There was 1 infant diagnosed as dysmature with birth weight 2,200 gm and EGA of 40 weeks. Of the small for gestational age (SGA) infants, 23% were twins.) Table II indicates the infant's diagnoses, and the majority, especially those occurring most frequently, are treatable. The severely and permanently damaging conditions (such as intracranial hemorrhage, cerebral palsy) are very few and affect about 1% o f all the infants. The 136 lower-weight prematures had a mean of 4 of the diagnoses listed in Table II during their stay in the Intensive Care Unit. The 136 upper-weight prematures had a mean of 2 of these diagnoses. For the 186 full-term infants, 78% had no illness, and most of the 22% who were ill had a single diagnosis. These data indicate that birth weight is associated with illness and hospital stay. As will be noted, the illnesses are now treatable. (Since the infants were seen in well-baby clinics, the figures for significant diagnoses for these infants should not be taken as representative of their weight groups and are probably underdiagnosed.)
Max Sugar
15
TABLE II PERCENTAGE'OF INFANTS' DIAGNOSESBY BIRTH WEIGHT
Diagnosis Strabismus Intracranial Hemorrhage Cerebral Palsy Hyperbilirubinemia Hypoglycemia Hypocalcemia Resp. Dist. Syndrome Cyanosis Apnoea Blood Incompatibility Pneumonia Hydrocephalus Microcephaly Anemia Cong. Heart Disease Major Surgery Major Infection Congenital Anomaly Exophthalmus Meningitis Hypothermia Atelectasis, Sickle Cell Anemia Spherocytosis Failure to Thrive Rubella Cataracts Retardation Club Foot Convulsive Disorder
Prematures 1250 gm N-136)
~
38 2 3 45 14 29 39 2 15 7 13 2 0 53 lO 15 17 18 3 3 l 2 2 1250 gm ~2501 gm (N,213) (N-186) 39 2 4
46 8 20 24 4
14 4 9 2 l 17 4
9 26 II 3 3 3 1250 mg >2501 gm
Weeks In Nursery
lO
5
0.7
First Exam In Weeks
14
I0
7
Smile, History
4
6
7
~mile, Exam
7
9
I0
Recognition of Mother's Voice
4
7
8
Recognition of Mother's Face
7
II
13
Following
7
t2
16
]5
18
19
23
Weeks At HomeBefore
Onset of:
Two Hand-Eye Coordination, History
II
Two Hand-Eye Coordination, Exam
14 J
I
Fraiberg [10] stated that the 3-month smile of the congenitally blind child is muted because of the lack of reinforcement. This may also be the case with the smile onset of prematures who remain in a nursery for 2 or 3 months, since their smile may not be reinforced in an intensive care nursery that keeps the mother out, and then a timorous, inexperienced mother may not recognize or reinforce the smile when it occurs at home. The onset of smile by history was based on the mother's statement (when confirmed suitably by me), which reflects the mother's achievement and strength of attachment to the infant. It is thus possible that the smile may take place even earlier than reported here. The data would seem to support a difference in accuracy of observations between early and later developmental milestones that seems
20
Child Psychiatry and Human Development
due to the method. Except for smiling, there is no statistical difference for these milestones' mean onset ages between premature and full-term infants, which indicates that there is no need to expect a delayed onset for these milestones in prematures. Neonatology. The figures for the milestones' onset may reflect general progress in neonatology with prevention and therapy of many conditions in the past decade or so, and thus the conclusions based on prematures, especially the ill ones, who were born two or more decades ago, may not be accurate or predictive n o w [ 1 1 - 1 5 ] . Since fetal conditioning is possible [16, 17], its effect, as well as the effects of imprinting [18] and earlier maternal bonding, on the onset of these milestones cannot be estimated in this study. Stimulation. Avery and Frantz [19] noted that fetal organs may differ in growth or development rates and have retardation or acceleration in either. Since myelinization depends on exercise [20], appropriate early stimulation may increase the rate of its development, and this seems to be confirmed by various recent authors [9, 16, 2124]. Saint-Anne Dargassies' studies [25] of neurological development in prematures were based on observations at birth of infants of various gestational ages, b u t did not include observations of the continued progressive neurological development of the infants for 6 months postnataily. It is almost as if the implication is that the infants' state at birth is an inevitable predictor of all future developments, or, as Gesell and Amatruda [1] state, that a premature never catches up. But Gesell and Amatruda's findings, and those of Lubchenco, Delivoria-Papadopoulos, and Searls [26] were based on prematures born in the 1950s, when prenatal and neonatal care were n o t as they are at present. By inference, according to these authors, it would appear that the premature born 5 or 10 weeks before term lies fallow until 40 weeks of age postconceptually, and then its development begins. This is to deny any effect of being alive or being suitably stimulated. Table V challenges this notion. Beyond the lack of opportunity, the differences may be related to the unevenness of prematures' stimulation of CNS development [27]. Investigations by Littman [28] stress that myelinization functions independently of the premature birth and major perinatal events; its extrauterine rates of development compared favorably with intrauterine rates; and that the neurological similarities " b e t w e e n prematures at term and term infants are much greater than the differences." Rice
Max Sugar
21
[ 29] has provided further data on the beneficial effects of stimulation on the general growth and neurological and mental development of prematures. In her studies, some of the prematures surpassed the full-terms in early developmental rate by EGA. I have no intention of minimizing the value of the gestational age, particularly in diagnosing a small-for-gestation, postmature, or dysmature infant. Although the EGAs were recorded incompletely, the data were comparable to those from the birth weight. In addition, both Rubin, Rosenblatt, and Balow [30] and Wiener [31] found that birth weight rather than gestational age was the major correlate of psychological, educational, and IQ development. These results provide empirical statistical support for the conclusion that the relationship o f these five milestones to weeks in the nursery is due to opportunity to observe them and n o t a causality that operates through biological factors represented by, or highly correlated with, birth weight or illness. A cautious approach is indicated toward the figures listed here, since with a more refined investigation with regular weekly observations in the nursery and in the home, the onset age of the milestones might even be found to be appreciably earlier. These milestones are not intended to reflect all the attainments of prematures or to indicate whether there is general acceleration or retardation of all milestones for prematures. These five milestones may be readily observed, and the figures offer additional guidelines for assessing the premature's development clinically. The most significant item to be considered from the figures is the direction they give to the expectation of normal onset age in prematures of these and possibly other developmental milestones. Conclusions
No statistical difference in the means was found for the onset of four of the five milestones in premature infants compared to fullterms. The statistical delay in smile onset seems due to the decreased observational opportunity during a lengthy hospital stay. Although some significant differences are present in the two- and 3-group tests, the basis for them and their application is unclear. These findings provide a clinical reference point for evaluation of these five milestones in prematures, using birth weight and length (which mothers are more likely to know and remember than gestational age) without adding a correction factor for gestational age. It is suggested that no correction factor need be added for these
22
Child Psychiatry and Human Development
five milestones, and if they are delayed, it would be due to some other cause than prematurity. In view of this, the concept of expected developmental retardation in prematures bears reexamination. Birth weight and length alone may be useful for observing the emergence of these five milestones in premature infants, since they are comparable to the data derived using EGA. The hypothesis that premature infants would have a delay in onset of these early milestones due to maternal separation is not validated in this study.
Summary The onset age for developmental milestones in premature infants was studied in 535 infants and was related to time of separation from their mothers. Since premature infants may be separated from their mothers for several months, it was hypothesized that the infants would show a delay in acquiring developmental milestones related to length of time separated from the mother. This report is on five early milestones: the development of two of these, recognition of mother's voice and recognition of mother's face, is related to time of separation from mother; the development of the other three milestones--the 3-month social smile response, visual following through 180 ~ and two handeye coordination--is not dependent on time of separation of infant from mother. Except for the onset of smiling, there was no statistically significant difference in the means between the premature and full-term infants. An effect from maternal separation was not demonstrated in the onset of these milestones. Birth weight and length seem to be reliable bases for the development of these milestones in premature infants, since their onset age is similar whether compared with gestational age or nursery stay groups.
References 1. Gesell AL, Amatruda CS: In H Knobloch & B. Pasamanick (Eds), Developmental Diagnoses (3rd ed). New York, Harper & Row, 1974. 2. Stuart HC: Physical growth and development. In HC Stuart & DG Prugh (Eds), The Healthy Child. Cambridge, Harvard University Press, 1964. 3. Hollingshead AB, Redlich FC: Social Class and Mental Illness. New York, Wiley, 1958.
Max Sugar
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4. Bowlby J: The nature of the child's tie to his mother. Int JPsychoanal 34: 1-23,1958. 5. Polak PR, Erode RN, Spitz RA: The smiling response to the h u m a n face, I: Methodology, quantification and natural history. J Nerv Ment Dis 139:103109, 1964. 6. McGraw MB: Neural maturation as exemplified in the reaching-prehensile behavior of the human infant. JPsychol 11:127-144, 1941. 7. Griffiths R: The Abilities o f Babies. New York, McGraw-Hill, 1954. 8. Watson EH, Lowrey GH: Growth and Development (3rd ed). Chicago, Yearbook Medical Publisher, 1958. 9. Klaus MH, Jereauld R, Kreger JC: Maternal attachment, importance of the first postpartum days. N Eng J Med 286:460-463, 1972. 10. Fraiberg S: Psychiatry and mental health. Presented at the American Academy of Child Psychiatry meeting, Toronto, October 1976. 11. Hobel CJ, Oh W, Hyvarinen MA, Emmanoulides GC, Erenberg A: Early versus late treatment of neonatal acidosis in low birth-weight infants: Relation to respiratory distress syndrome. J Pediatr 81 : 1178-1187,1972. 12. Koivisto J, Blanco-Sequeiros M, Kraus U: Neonatal symptomatic and asymptomatic hypoglycemia. Dev Med Child Neuro114:603-614, 1972. 13. Medical World News, August 4, 1972, pp 44-51. 14. Stewart A: The risk of h~indicap due to birth defect in infants of very low birth-weight. Dev Med Child Neurol 14:585-591, 1972. 15. Upadhyay Y: A longitudinal study of full-term neonates with hyperbilirubinemia to four years of age. Johns Hopkins Med J 128:273-277, 1971. 16. Liley AW: The foetus as a personality. Aust N Z JPsychiatry 6:99-105, 1972. 17. Spelt DK: The conditioning of the human fetus in utero. J E x p Psychol 38: 338-346, 1948. 18. Salk L: The mother's heart beat as an imprinting stimulus. Trans N Y Acad Sci, Series II, 24:753-763, 1962. 19. Avery ME, Frantz I: Commentary: Intrauterine developmental retardation. J Pediatr 87:956-957, 1975. 20. Beckoff M, Fox MW: Postnatal neural ontogeny: Environment-dependent and/or environment expectant? Dev Psychobio 5:323-341, 1971. 21. Powell LF: The effect of extra stimulation and maternal involvement on the development of low-birth-weight infants and on maternal behavior. Child Dev 45:106-113, 1974. 22. Scarr-Salapatek S, Williams ML: The effects of early stimulation on lowbirth-weight infants. Child Dev 44:94-101, 1973. 23. Freedman DA: Congenital and perinatal sensory deprivation: Their effect on the capacity to experience affect. Psychoanal Q 44:62-81, 1975. 24. Sugar M: Premature and full-term infant-caretaker interactions. Presented at the 8th International Congress of Child Psychiatry, Philadelphia, July 1974. 25. Saint-Anne Dargassies S: Neurological maturation of the premature infant of 28 to 41 weeks gestational age. In F Fauikner (Ed), Human Development. Philadelphia, Saunders, 1966. 26. Lubchenco LO, Delivoria-Papadopoulos M, Searls D: Long-term follow-up studies of prematurely born infants, II: Influence of birth weight and gestational age on sequelae. JPediatr 80:509-512, 1972. 27. Rose SA, Schmidt K, Bridger WH: Cardiac and behavioral responsivity to tactile stimulation in premature and full-term infants. Presented at the meeting of the Society for Research in Child Development, Denver, April 1975. 28. Littman B: Prematurity, peripheral nerve myelination and the measurement of conceptional age. Presented at the meeting of the Society for Research in Child Development, Denver, April 1975.
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Child Psychiatry and Human Development
29. Rice RD: Premature infants respond to sensory stimulation. Presented at the meeting of the American Psychological Association, Chicago, September 1975. 30. Rubin RA, Rosenblatt C, Balow B: Psychological and educational sequelae of prematurity. Pediatrics 52: 352-363, 1973. 31. Wiener G: Scholastic achievement at age 12-13 of prematurely born infants. J Special Education 2: 237-250, 1968.
The onset of five early milestones was studied in premature and full-term infants. The milestones are: recognition of mother's voice and face, 3month smile, following through 180 ~ and two hand-eye coordination. It was hypothesized that premature infants would show delay in acquiring milestones related to time separated from mother. Compared to full-term infants, the prematures had a significant difference in the means only for the onset of smiling, and no effect related to maternal separation.
ABSTRACT:
Reported comparisons of premature and full-term infants have been based on psychological and educational achievements involving extensive testing. No age is given for the appearance of developmental milestones in premature infants, except to add a correction factor based on gestational age [ 1 : 2 5 5 ] . A clinical guideline of expectations for premature infants' milestones that may be observed easily might be useful in assessing some aspects of the premature infant's development. This paper, part of a longitudinal study of milestones in prematures in the first 2 years of life, reports on five such milestones in the first 6 months postdelivery. These are the onset age of 3-month smiling, following, t w o hand-eye coordination, recognition of mother's voice, and recognition of mother's face. It was hypothesized that since prematures may be separated from Dr. Sugar is Clinical Professor of Psychiatry, Louisiana State University School of Medicine, New Orleans, Louisiana. Address reprint requests to Dr. Sugar, 17 Rosa Park, New Orleans, Louisiana 70115. The author is grateful to Juan-Washington, MD, former Director, and his staff, of the Newborn Intensive Care Unit, and to the Premature Outpatient Clinic of Charity Hospital in New Orleans for their excellent cooperation during this study; M. Kelly, RN, former Director, and her staff, at the Mary Buck City Health Clinic; Lawrence Van Egeren, PhD, and Lawrence Weber, PhD, for help with the statistics; David Taylor for the computer programming; David A. Freedman, MD, and Gerald Wiener, PhD, for their critical reading of the manuscript. Child Psychiatry and Human Development
Vol. 8(1), Fall 1977
11
12
Child Psychiatry and Human Development
t h e i r m o t h e r s f o r several m o n t h s , t h e y w o u l d s h o w delay in acquiring d e v e l o p m e n t a l m i l e s t o n e s r e l e a t e d t o t i m e o f s e p a r a t i o n f r o m the m o t h e r . T w o o f t h e m i l e s t o n e s - - r e c o g n i t i o n o f m o t h e r ' s voice a n d f a c e - - a r e t h e o r i z e d t o be i n t i m a t e l y involved in t h e a t t a c h m e n t p r o c ess a n d require t h e m o t h e r ' s p r e s e n c e f o r their d e v e l o p m e n t . F o r the d e v e l o p m e n t o f the o t h e r t h r e e m i l e s t o n e s - - 3 - m o n t h smile, following, a n d t w o h a n d - e y e c o o r d i n a t i o n - - i t is felt t h a t t h e regular and c o n s t a n t p r e s e n c e o f a significant p a r e n t i n g figure is n o t n e e d e d . A c o m p a r i s o n o f o n s e t ages in t h e s e t w o g r o u p s with t h e i r d i s p a r a t e relation to the a t t a c h m e n t p r o c e s s m i g h t d i f f e r e n t i a t e the e f f e c t s o f m a t e r n a l s e p a r a t i o n due to a l e n g t h y n u r s e r y stay f r o m biological c o n t r i b u t i o n s to t h e d e v e l o p m e n t o f these m i l e s t o n e s . E a c h o f these i t e m s t h u s has i m p o r t a n c e as an a c h i e v e m e n t b y the i n f a n t a n d as a s t i m u l u s to the m o t h e r in her p l e a s u r a b l e i n v o l v e m e n t with t h e i n f a n t a n d its d e v e l o p m e n t .
Method After the first months, some pediatricians may calculate the onset of all milestones by estimated gestational age (EGA) for low birth weight infants, but my impression is that generally they use birth weight for expectations of development for all infants. Thus, the focal point here is the birth weight, since this was recorded regularly and determined the prematures' discharge from the Newborn Intensive Care Unit. Since the gestational age was irregularly noted on the charts and its accuracy questionable, while the birth weight and length were routinely recorded, the definition of prematurity used here is a birth weight of 2,500 gm or less with a birth length of 47 cm or less (heel to crown) and (whenever noted) an EGA of 37 weeks or less [2:99]. In this paper, for brevity, birth weight of < 2,500 gm will also refer to birth length of < 47 cm. The infants were divided into groups by birth weight, EGA, and nursery stay as follows: (a) birth weight--as prematures of < 1,250 gm with < 47 cm length; > 1,250 gm but < 2,500 gin, with < 47 cm length; and a full-term group > 2,500 gm with > 47 cm length; (b) EGA--as < 32 weeks' gestation, < 37 weeks' gestation, and ~ 38 weeks' gestation; and (c) length of nursery stay--as > 7 weeks, 3 to 7 weeks, and < 2 weeks. Onset age for the milestones here is the chronological age after birth for all the infants. This allows the postdelivery onset age of the milestones to be determined in prematures and full-terms and for the two groups to be compared. A coeval determination is possible of the effects, if any, of maternal separation from the infant on the development of the milestones. In this study, the infants were born between 1969 and 1975. The mothers of the premature and full-term infants were separated from them and uninvolved in their care until discharge from the municipal hospital. Premature infants were discharged from the N.I.C.U. when stabilized and weighing about 41/~pounds.
Max Sugar
13
TABLE I SCORING OF THE MILESTONES
Milestones
Average Onset Age (Range is 2 months)a
Upper Age I Limit f o r Inclusion b
Stimuli Used
Presence, Duration and/or Confirmation of Milestone
3-Months Smile (3,4)
3 months
20 weeks Observer' s, other's Present for or mother's voice, l second and face (with mouth repeatable.c, d open or smiling or moving), face-mask, l i g h t or bell.
Following (3)
4 months
24 weeks Any slowly moving object in visual field.
Follows slowlymoving object with head and eyes through arc of 180v and repeatable, d
2 Hand-Eye Coordination (51
7 months
38 weeks Any object that is i n v i t i n g and capable of being grasped with 2 hands.
Grasping with 2 hands in response to visual stimulus and repeatable~,d
Recognition of Mother's Voice (6)
12 weeks
20 weeks
Mother's or mothering person's voice with face out of view.
Recognition of Mother's Face (7)
12 weeks
20 Mother's face weeks without speech.
Smiling, being soothed, discontinued crying or recognition response only to mother's voice and repeatable,c Smiling, being soothed, discontinued crying or recognition response only to mother's face and
repeatable, c
aAs derived from l i t e r a t u r e cited in the l e f t hand column. bIf not present at exam before upper age l i m i t , but had monthly exams therea f t e r , then scored as of date observed; otherwise, scored as "no data" for that milestone for the infant. CBased on mother's history i f confirmed on exam within l month of her date. dBased on exam i f seen at least once before upper age and then monthly.
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Child Psychiatry and Human Development
The infants in this study were seen in the premature clinic of the local municipal hospital or at a city health clinic. Beginning 2 weeks after hospital discharge, the premature infants routinely came to the premature clinic monthly until 6 months of age, then bimonthly until age I year, then semiannually until 3 years of age, and annually thereafter. Full-term infants and a few prematures were observed at the neighborhood city health clinic, which offered routine well-baby examinations for all newborns in the area beginning at 4 days, then on a monthly basis for the first year, then every 3 months for the second year. Socioeconomically, the city health clinic had a population similar to that of the municipal hospital, and most o f the infants were delivered at this hospital. The premature and full-term groups were similar in both clinics socioeconomically and racially, with 91% of both groups of lower socioeconomic status (note that lower S.E.S. conforms to the definition for classes 4 and 5 of Hollingshead and Redlich [3] ) and 9% middle S.E.S. made up of 90% black and 10% white infants. Criteria for scoring each milestone are listed in Table I [ 4 - 8 ] . The total population consisted of 535 infants divided by birth weight and as follows: 349 p r e m a t u r e s - 136 prematures weighing 1,250 gm or less (mean 1,036, S.D. 159) and 213 prematures weighing ove~ 1,250 gm (mean 1751, S.D. 345); 186 full-term infants weighing over 2,500 gm (mean 3,282, S.D. 454). There were many drop-outs and infants' visits often did not meet the criteria for time limits indicated above. Thus, the numbers reported on for each milestone noted in the tables differ somewhat, but they meet the requirements listed in Table I, and there are about 50 for each milestone in each weight group. Among the total o f 535 infants, there were 49 from multiple births from different weight categories as follows: 17 in the lower-weight prematures, 29 in the upper-weight prematures, and 3 in the full-term group. In some multiple births, the twinship had been lost through death at birth or neonatally as follows by weight: < 1,250 gm --13 infants; > 1,250 gin--none; full-term--3 infants. The mean gestational age for the smaller prematures--< 1,250 gm (136) of whom 112 had EGA recorded-was 29 weeks (S.D. 2.9); for the large prematures--> 1,250 gm (213) of whom 160 had EGA recorded--was 34 weeks (S.D. 3.1); and for the 186 full-terms--> > 2,500 gin, EGA recorded--was 40 weeks (S.D. 0.0). These figures are an indication of poor recording for EGA. (There were 13 infants diagnosed as small for gestational age; 6 were < 1,250 gm with EGA range 28 to 40 weeks, and 7 were > 1,250 gm with EGA range of 30 to 40 weeks. There was 1 infant diagnosed as dysmature with birth weight 2,200 gm and EGA of 40 weeks. Of the small for gestational age (SGA) infants, 23% were twins.) Table II indicates the infant's diagnoses, and the majority, especially those occurring most frequently, are treatable. The severely and permanently damaging conditions (such as intracranial hemorrhage, cerebral palsy) are very few and affect about 1% o f all the infants. The 136 lower-weight prematures had a mean of 4 of the diagnoses listed in Table II during their stay in the Intensive Care Unit. The 136 upper-weight prematures had a mean of 2 of these diagnoses. For the 186 full-term infants, 78% had no illness, and most of the 22% who were ill had a single diagnosis. These data indicate that birth weight is associated with illness and hospital stay. As will be noted, the illnesses are now treatable. (Since the infants were seen in well-baby clinics, the figures for significant diagnoses for these infants should not be taken as representative of their weight groups and are probably underdiagnosed.)
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TABLE II PERCENTAGE'OF INFANTS' DIAGNOSESBY BIRTH WEIGHT
Diagnosis Strabismus Intracranial Hemorrhage Cerebral Palsy Hyperbilirubinemia Hypoglycemia Hypocalcemia Resp. Dist. Syndrome Cyanosis Apnoea Blood Incompatibility Pneumonia Hydrocephalus Microcephaly Anemia Cong. Heart Disease Major Surgery Major Infection Congenital Anomaly Exophthalmus Meningitis Hypothermia Atelectasis, Sickle Cell Anemia Spherocytosis Failure to Thrive Rubella Cataracts Retardation Club Foot Convulsive Disorder
Prematures 1250 gm N-136)
~
38 2 3 45 14 29 39 2 15 7 13 2 0 53 lO 15 17 18 3 3 l 2 2 1250 gm ~2501 gm (N,213) (N-186) 39 2 4
46 8 20 24 4
14 4 9 2 l 17 4
9 26 II 3 3 3 1250 mg >2501 gm
Weeks In Nursery
lO
5
0.7
First Exam In Weeks
14
I0
7
Smile, History
4
6
7
~mile, Exam
7
9
I0
Recognition of Mother's Voice
4
7
8
Recognition of Mother's Face
7
II
13
Following
7
t2
16
]5
18
19
23
Weeks At HomeBefore
Onset of:
Two Hand-Eye Coordination, History
II
Two Hand-Eye Coordination, Exam
14 J
I
Fraiberg [10] stated that the 3-month smile of the congenitally blind child is muted because of the lack of reinforcement. This may also be the case with the smile onset of prematures who remain in a nursery for 2 or 3 months, since their smile may not be reinforced in an intensive care nursery that keeps the mother out, and then a timorous, inexperienced mother may not recognize or reinforce the smile when it occurs at home. The onset of smile by history was based on the mother's statement (when confirmed suitably by me), which reflects the mother's achievement and strength of attachment to the infant. It is thus possible that the smile may take place even earlier than reported here. The data would seem to support a difference in accuracy of observations between early and later developmental milestones that seems
20
Child Psychiatry and Human Development
due to the method. Except for smiling, there is no statistical difference for these milestones' mean onset ages between premature and full-term infants, which indicates that there is no need to expect a delayed onset for these milestones in prematures. Neonatology. The figures for the milestones' onset may reflect general progress in neonatology with prevention and therapy of many conditions in the past decade or so, and thus the conclusions based on prematures, especially the ill ones, who were born two or more decades ago, may not be accurate or predictive n o w [ 1 1 - 1 5 ] . Since fetal conditioning is possible [16, 17], its effect, as well as the effects of imprinting [18] and earlier maternal bonding, on the onset of these milestones cannot be estimated in this study. Stimulation. Avery and Frantz [19] noted that fetal organs may differ in growth or development rates and have retardation or acceleration in either. Since myelinization depends on exercise [20], appropriate early stimulation may increase the rate of its development, and this seems to be confirmed by various recent authors [9, 16, 2124]. Saint-Anne Dargassies' studies [25] of neurological development in prematures were based on observations at birth of infants of various gestational ages, b u t did not include observations of the continued progressive neurological development of the infants for 6 months postnataily. It is almost as if the implication is that the infants' state at birth is an inevitable predictor of all future developments, or, as Gesell and Amatruda [1] state, that a premature never catches up. But Gesell and Amatruda's findings, and those of Lubchenco, Delivoria-Papadopoulos, and Searls [26] were based on prematures born in the 1950s, when prenatal and neonatal care were n o t as they are at present. By inference, according to these authors, it would appear that the premature born 5 or 10 weeks before term lies fallow until 40 weeks of age postconceptually, and then its development begins. This is to deny any effect of being alive or being suitably stimulated. Table V challenges this notion. Beyond the lack of opportunity, the differences may be related to the unevenness of prematures' stimulation of CNS development [27]. Investigations by Littman [28] stress that myelinization functions independently of the premature birth and major perinatal events; its extrauterine rates of development compared favorably with intrauterine rates; and that the neurological similarities " b e t w e e n prematures at term and term infants are much greater than the differences." Rice
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[ 29] has provided further data on the beneficial effects of stimulation on the general growth and neurological and mental development of prematures. In her studies, some of the prematures surpassed the full-terms in early developmental rate by EGA. I have no intention of minimizing the value of the gestational age, particularly in diagnosing a small-for-gestation, postmature, or dysmature infant. Although the EGAs were recorded incompletely, the data were comparable to those from the birth weight. In addition, both Rubin, Rosenblatt, and Balow [30] and Wiener [31] found that birth weight rather than gestational age was the major correlate of psychological, educational, and IQ development. These results provide empirical statistical support for the conclusion that the relationship o f these five milestones to weeks in the nursery is due to opportunity to observe them and n o t a causality that operates through biological factors represented by, or highly correlated with, birth weight or illness. A cautious approach is indicated toward the figures listed here, since with a more refined investigation with regular weekly observations in the nursery and in the home, the onset age of the milestones might even be found to be appreciably earlier. These milestones are not intended to reflect all the attainments of prematures or to indicate whether there is general acceleration or retardation of all milestones for prematures. These five milestones may be readily observed, and the figures offer additional guidelines for assessing the premature's development clinically. The most significant item to be considered from the figures is the direction they give to the expectation of normal onset age in prematures of these and possibly other developmental milestones. Conclusions
No statistical difference in the means was found for the onset of four of the five milestones in premature infants compared to fullterms. The statistical delay in smile onset seems due to the decreased observational opportunity during a lengthy hospital stay. Although some significant differences are present in the two- and 3-group tests, the basis for them and their application is unclear. These findings provide a clinical reference point for evaluation of these five milestones in prematures, using birth weight and length (which mothers are more likely to know and remember than gestational age) without adding a correction factor for gestational age. It is suggested that no correction factor need be added for these
22
Child Psychiatry and Human Development
five milestones, and if they are delayed, it would be due to some other cause than prematurity. In view of this, the concept of expected developmental retardation in prematures bears reexamination. Birth weight and length alone may be useful for observing the emergence of these five milestones in premature infants, since they are comparable to the data derived using EGA. The hypothesis that premature infants would have a delay in onset of these early milestones due to maternal separation is not validated in this study.
Summary The onset age for developmental milestones in premature infants was studied in 535 infants and was related to time of separation from their mothers. Since premature infants may be separated from their mothers for several months, it was hypothesized that the infants would show a delay in acquiring developmental milestones related to length of time separated from the mother. This report is on five early milestones: the development of two of these, recognition of mother's voice and recognition of mother's face, is related to time of separation from mother; the development of the other three milestones--the 3-month social smile response, visual following through 180 ~ and two handeye coordination--is not dependent on time of separation of infant from mother. Except for the onset of smiling, there was no statistically significant difference in the means between the premature and full-term infants. An effect from maternal separation was not demonstrated in the onset of these milestones. Birth weight and length seem to be reliable bases for the development of these milestones in premature infants, since their onset age is similar whether compared with gestational age or nursery stay groups.
References 1. Gesell AL, Amatruda CS: In H Knobloch & B. Pasamanick (Eds), Developmental Diagnoses (3rd ed). New York, Harper & Row, 1974. 2. Stuart HC: Physical growth and development. In HC Stuart & DG Prugh (Eds), The Healthy Child. Cambridge, Harvard University Press, 1964. 3. Hollingshead AB, Redlich FC: Social Class and Mental Illness. New York, Wiley, 1958.
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4. Bowlby J: The nature of the child's tie to his mother. Int JPsychoanal 34: 1-23,1958. 5. Polak PR, Erode RN, Spitz RA: The smiling response to the h u m a n face, I: Methodology, quantification and natural history. J Nerv Ment Dis 139:103109, 1964. 6. McGraw MB: Neural maturation as exemplified in the reaching-prehensile behavior of the human infant. JPsychol 11:127-144, 1941. 7. Griffiths R: The Abilities o f Babies. New York, McGraw-Hill, 1954. 8. Watson EH, Lowrey GH: Growth and Development (3rd ed). Chicago, Yearbook Medical Publisher, 1958. 9. Klaus MH, Jereauld R, Kreger JC: Maternal attachment, importance of the first postpartum days. N Eng J Med 286:460-463, 1972. 10. Fraiberg S: Psychiatry and mental health. Presented at the American Academy of Child Psychiatry meeting, Toronto, October 1976. 11. Hobel CJ, Oh W, Hyvarinen MA, Emmanoulides GC, Erenberg A: Early versus late treatment of neonatal acidosis in low birth-weight infants: Relation to respiratory distress syndrome. J Pediatr 81 : 1178-1187,1972. 12. Koivisto J, Blanco-Sequeiros M, Kraus U: Neonatal symptomatic and asymptomatic hypoglycemia. Dev Med Child Neuro114:603-614, 1972. 13. Medical World News, August 4, 1972, pp 44-51. 14. Stewart A: The risk of h~indicap due to birth defect in infants of very low birth-weight. Dev Med Child Neurol 14:585-591, 1972. 15. Upadhyay Y: A longitudinal study of full-term neonates with hyperbilirubinemia to four years of age. Johns Hopkins Med J 128:273-277, 1971. 16. Liley AW: The foetus as a personality. Aust N Z JPsychiatry 6:99-105, 1972. 17. Spelt DK: The conditioning of the human fetus in utero. J E x p Psychol 38: 338-346, 1948. 18. Salk L: The mother's heart beat as an imprinting stimulus. Trans N Y Acad Sci, Series II, 24:753-763, 1962. 19. Avery ME, Frantz I: Commentary: Intrauterine developmental retardation. J Pediatr 87:956-957, 1975. 20. Beckoff M, Fox MW: Postnatal neural ontogeny: Environment-dependent and/or environment expectant? Dev Psychobio 5:323-341, 1971. 21. Powell LF: The effect of extra stimulation and maternal involvement on the development of low-birth-weight infants and on maternal behavior. Child Dev 45:106-113, 1974. 22. Scarr-Salapatek S, Williams ML: The effects of early stimulation on lowbirth-weight infants. Child Dev 44:94-101, 1973. 23. Freedman DA: Congenital and perinatal sensory deprivation: Their effect on the capacity to experience affect. Psychoanal Q 44:62-81, 1975. 24. Sugar M: Premature and full-term infant-caretaker interactions. Presented at the 8th International Congress of Child Psychiatry, Philadelphia, July 1974. 25. Saint-Anne Dargassies S: Neurological maturation of the premature infant of 28 to 41 weeks gestational age. In F Fauikner (Ed), Human Development. Philadelphia, Saunders, 1966. 26. Lubchenco LO, Delivoria-Papadopoulos M, Searls D: Long-term follow-up studies of prematurely born infants, II: Influence of birth weight and gestational age on sequelae. JPediatr 80:509-512, 1972. 27. Rose SA, Schmidt K, Bridger WH: Cardiac and behavioral responsivity to tactile stimulation in premature and full-term infants. Presented at the meeting of the Society for Research in Child Development, Denver, April 1975. 28. Littman B: Prematurity, peripheral nerve myelination and the measurement of conceptional age. Presented at the meeting of the Society for Research in Child Development, Denver, April 1975.
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Child Psychiatry and Human Development
29. Rice RD: Premature infants respond to sensory stimulation. Presented at the meeting of the American Psychological Association, Chicago, September 1975. 30. Rubin RA, Rosenblatt C, Balow B: Psychological and educational sequelae of prematurity. Pediatrics 52: 352-363, 1973. 31. Wiener G: Scholastic achievement at age 12-13 of prematurely born infants. J Special Education 2: 237-250, 1968.
