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The early social environment of premature and fullterm infants
Early Human Development, 17 (1988) 221--232
221
Elsevier Scientific Publishers Ireland Ltd. EHD 00904
The early social environment of premature and fullterm infants D i a n e H o l d i t c h D a v i s a n d E v e l y n B. T h o m a n Department o f Biobehavioral Sciences, The University of Connecticut, Storrs, CT 06268, U.S.A. Accepted for publication 12 November 1987
Summary The behaviors of 10 mothers of prematures and 29 mothers of fullterms were compared from 7-h observations made in the home when the infants were 2, 3, 4 and 5 weeks post-term. The observation day was divided into four mutually exclusive interactional contexts that together made up the total day: feeding time, changing or bathing time, time when the mother and infant were in physical contact but the mother was not caretaking, and time the infant was alone. Measures of ten maternal behaviors were also compared: moving, rocking, patting, caressing, talking, looking, engaging in vis-a-vis with the baby, holding or carrying, smiling or laughing, and stimulating the baby to suck. Mothers of prematures left their infants alone more and changed them less than mothers of fullterms. In addition, mothers of prematures moved their infants less often, talked to their infants less, looked at their infants less, and held their infants less. These results indicate that, over the 7-h day, prematures receive markedly less stimulation than fullterms. Since the neurobehavioral characteristics of premature and fullterm infants are known to differ [15], it is suggested that these differences in maternal behaviors may be in response to infant cues and appropriate for the infants. premature infants; infants; mothers; mother-infant interaction; social environment
Introdution The role of the social environment in the development of premature infants has received considerable attention [7,13,40]. Studies indicate that it may be an important factor in the developmental course of these vulnerable infants. For Address for correspondence: Diane Holditch Davis, School of Nursing, CB No. 7460 Carrington Hall, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599-7460, U.S.A. 0378-3782/88/$03.50 © 1988 Elsevier Scientific Publishers Ireland Ltd. Published and Printed in Ireland
222 example, Sameroff and Chandler reported that infant outcome is more directly related to the social environment than to adverse perinatal experiences [40]. Cohen and Beckwith have suggested that optimal maternal stimulation may be able to ameliorate the effects of perinatal stresses; whereas, inappropriate stimulation may actually worsen these effects [13]. A number of recent studies have explored the early hospital environment of premature infants and, in particular, the types of stimulation they receive from their caregivers in the hospital [19,23,24,29,35]. However, the home environment of prematures in the first few months after hospital discharge and the stimulation they receive from caregivers in the home has received less attention. Interactions between prematures and their mothers during this early post-term period have most often been studied in the laboratory, an environment that might alter the nature of the interaction; and the few studies conducted in the home have generally been limited to a single interactional situation. Yet, behaviors in a single situation may not be typical of the whole relationship. With these variations in social situation, it is not surprising that the results of studies of the early behaviors of mothers of prematures have been contradictory. Some reports indicate that mothers of prematures display less positive affect toward the infant [14,17,21,30] and less synchrony in their interactions [27,31]. Other studies have found that mothers of prematures cuddle their infants less [30], talk to their infants less [4,5,17], and touch their infants less [3,14,17,30]. Still other studies have found that mothers of premature infants are more active in initiating and maintaining interactions [3,4,20]. In still other studies, the behaviors of mothers of prematures have been found not to differ from those of mothers of fullterms in the early weeks after term [1,28]. Thus, generalizations about the nature of premature mothering are still difficult. The purpose of this study was to describe the early social environment of premature infants, including the types of stimulation they receive from their mothers, over the range of circumstances that typically occur in the home. These social experiences of prematures were compared with those of healthy fullterm infants. Prolonged, naturalistic observations were made in the home when the infants were 2, 3, 4 and 5 weeks post-term, and the maternal behaviors were observed for a 7-h period each week. The way the mothers allocated their time to different social situations was determined by dividing the 7-h day into four mutually exclusive interactional contexts: Feeding, Change or Bathe, Social Contact, and Baby Alone. These interactional contexts were chosen because a previous study of fuUterm infants had indicated that they reliably discriminate among individuals and show predictive validity [44]. Measures of ten specific maternal behaviors were also examined. Methods
Subjects The subjects for this study were 10 premature infants and 29 fullterm infants who were enrolled in the Connecticut Longitudinal Project, a research study that
223 was approved by the institutional review boards of all participating hospitals [42,45,46]. Subjects, both premature and fullterm, were selected based on their availability at the time the laboratory was free to enroll a new subject and the willingness of the mother to be involved in the study. Mothers of both groups of infants gave informed consent for the study prior to their infant's discharge from the hospital. Fullterm subjects were recruited during the last month of pregnancy or during the postnatal hospitalization period. The only criterion for the selection of fullterm infants was that they have uncomplicated perinatal courses. The premature infants were enrolled during the preterm period after their medical conditions had stabilized. The selection criteria for these infants were that they were born at least 4 weeks prior to their obstetrical due dates and would be discharged home by 1 week post-term so that they would be available for home observations at the same post-term ages as the fullterms. (In actuality, all of the prematures in this study were discharged home before their term date.) The prematures had experienced a wide variety of medical courses, ranging from no complications and discharge home in the first week to respiratory distress syndrome and mechanical ventilation, but all were judged by pediatric examination to be healthy premature infants by the time of hospital discharge. These criteria were chosen so that a heterogeneous group of premature infants, representative of the vast majority of prematures who leave the hospital without obvious disabilities would be studied. Infants in both groups were Caucasian, single births, and average weight for gestational age. Five of the premature infants and 12 of the fullterms were secondborn and had an older fullterm sibling. The fullterm infants were discharged within 5 days after birth, and all prematures were discharged prior to their estimated term dates (mean 25 days). The parents of both groups were married, lived in single family homes, and were of lower middle to middle income levels. The infants were cared for primarily by their mothers with the exception of one premature infant who was cared for by a grandmother during the day. The demographic characteristics of the two groups of infants are given in Table I. The gestational ages of the infants were calculated from the obstetric estimated date of confinement which had been determined from either the date of the mother's last menstrual period of from ultrasound examinations. All of the gestational ages agreed within 2 weeks with the results of Dubowitz examinations [18] performed within 48 h of birth, and all fullterm infants had scores within 2 weeks of 40 weeks gestational age.
Procedures for observations This report is based on 7-h observations made in the home from approx. 0900 h to 1600 h when the infants were 2, 3, 4 and 5 weeks post-term. The mothers were familiar with the observational procedures because they and their infants had been observed together prior to the first observation in the present study. Mother and infant behaviors were recorded on a code sheet every 10 s throughout the observation. The end of each 10-s epoch was signaled through an ear phone from a small electronic timing device. At this signal, the observer wrote the codes for all variables
224 TABLE I Demographic characteristics of the premature and fuUterm infants. Prematures Mean Males/females First-/second-born Gestational age (weeks) Birth weight (g) Maternal age (years) Obstetric complicationsa Vaginal delivery/cesarean section l-rain Apgar 5-rain Apgar Neonatal complicationsb
5/5 5/5 31 1520 26 8.5 5/5 6.2 7.7 2.5
Fullterms Range
28--35 1260--2100 16--33 3-- 11 2--10 6--10 0--6
Mean 17/12 17/12 40 3536 26 3.1 28/1 8.9 9.7 0.2
Range
37--42 2750--4395 21 --34 2--6 7--10 9--10 0-- 1
aScored on Prechtl Scale [38]. Possible number of non-optimal events ranges from 0 to 42. bScored on Postnatal Complications Form [321. Possible number of non-optimal events ranges from 0 to 10.
occurring during the epoch on a sheet of paper. The observer remained in the room with the infant throughout the 7-h day recording maternal and infant behaviors. Each observation was shared by two observers, each recording for approx. 3.75 h. The changing of observers in the middle of the observation was accomplished without interruption of either the observational procedures or the ongoing household activities. The two observers recorded for a 15-rain overlap period so that ongoing reliability could be assessed. Inter-rater reliability for each variable was calculated for all observers on an ongoing basis, using this formula: 2 x number of epochs with agreements number of epochs recorded by observer 1 + observer 2 A minimum overall agreement of 85 % was maintained. Variables used f o r data analyses Interactional contexts. The observation was divided into four mutually exclusive interactional contexts which together made up the total observation day: (i) Feeding
the mother is either feeding the baby by breast, bottle, or spoon or is pausing briefly (< 10 rain) in the middle of a feeding, as for burping. (ii) C h a n g e or B a t h e - the mother is changing or bathing the baby. (iii) Social Contact ~ the mother is in physical contact with the baby (i.e., holding or touching) but is not feeding, changing, or bathing. (iv) B a b y A l o n e ~ the infant is not being held or touched by the mother.
225 M a t e r n a l b e h a v i o r s . Ten social behaviors were recorded in any epoch in which they occurred. Multiple occurrences of the same behavior in the same epoch were not recorded. These variables were defined as follows: (i) M o v e ~ The mother moves the baby so as to change the baby's position in space. (ii) R o c k - - the mother rocks the baby for at least two cycles. (iii) P a t - - The mother pats the baby. (iv) C a r e s s ~ The mother touches the baby in a light, non-rhythmic manner, such as strokes, kisses, nuzzles, wipes, tickles, and hand holding. (v) T a l k - - The mother talks to the infant. (vi) L o o k ~ The mother looks at the infant. (vii) Vis-a-Iris The mother and baby look at each other and have eye to eye contact. (viii) H o l d o r C a r r y ~ The mother is holding or carrying the infant. (ix) S m i l e o r L a u g h ~ The mother smiles or laughs at the baby. (x) S u c k S t i m u l a t e - - The mother moves the breast, bottle, pacifier, or her finger to elicit sucking. The stimulation provided on rare occasions by caregivers other than the mother was included in the maternal behaviors analyzed, as the focus of this study was the social experiences of the infants. Measures o f variables
The four interactional context and the ten maternal behaviors were each measured as a percentage of the total observation time. Each maternal behavior was also measured as a percentage of the time the infants were in physical contact with their mother (i.e. during Feeding, Change or Bath, and Social Contact). Statistical analyses
One fullterm and three premature infants were each missing one observation. The missing values were estimated using the procedure described in Winer [49, see pp. 487--488]. these estimates were used in all of the analyses described in this paper. The degrees of freedom were appropriately reduced to compensate for these estimations. I n d i v i d u a l d i f f e r e n c e s . Individual differences for the interactional contexts and the maternal variables were assessed separately for the fullterm and premature infants using a two-factor repeated measures analysis of variance for each variable. The ANOVA included the following sources of variance: Sex, Subjects, Weeks, Sex by Weeks, and Subjects by Weeks. To test for individual differences, the Mean Square for Subjects was divided by the Mean Square for Subjects by Weeks with the assumption that Weeks is a random variable [16,49]. G r o u p c o m p a r i s o n s . The percentage of the total observation that the mothers of the prematures and fullterms spent in each of the interactional contexts and in each maternal behavior was compared by using a repeated measures analysis of variance for each variable. Three-factor (Group by Birth Order by Week) ANOVAs were used for the interactional contexts, and four-factor (Group by Birth Order by Context by Week) ANOVAs for the social behaviors. In addition, each maternal behavior was measured as a percentage of the time the infants were in physical contact with their mothers. The two groups of infants were compared using three-factor (Group by Birth Order by Week) repeated measures ANOVA for each of these variables. The Birth Order factor was included in each of these analyses to account for
226 the possibility that mothers of premature and fullterm infants might respond differently as a function of the infant's birth order. Because of the difference in the sample size of the two groups, each analysis of variance used an unweighted means procedure, thereby giving equal weight to the means of the two groups rather than giving greater weight to the group with the larger sample size. Since the variances of five of the ten maternal variables and two of the interactional contexts were significantly greater for the fullterms than for the premature infants, the mean differences were also calculated using (i) the Mann-Whitney non-parametric test and (ii) a conservative F-test using the larger variance for the error term with its associated degrees of freedom. In all instances in which the primary analysis found significant main effects, these tests also found significance. Relation between neonatal complications and maternal behaviors. To determine whether the amount of neonatal complications affects the maternal behaviors of premature infants, correlations between the number of neonatal complications, as measured on the Postnatal Complications Scale [32], and the amount of each interactional context and maternal behavior were calculated for the group of premature infants. Results
Individual differences Table II presents the results of the individual differences analyses for the fullterm and premature infants. Significant individual differences were found for the amounts of time allocated to each variable for the fullterms. Despite the smaller number of subjects in the premature group, two of the interactional contexts and eight of the maternal behaviors exhibited significant individual differences. Two other variables approached significance. Time spent in each context by the prematures and fullterms Table II also presents the amounts of the interactional contexts averaged over the 4 weeks for the two groups of infants and the results of analyses comparing the amounts of these variables for premature and fullterm infants. The premature infants spent significantly more time in Baby Alone than the fullterms (F(1, 35) = 6.39, P < 0.05) and significantly less time in Change or Bathe (F(1, 35) = 6.70, P < 0.05). The lesser amount of Social Contact for the prematures approached significance (F(I, 35) = 3.79, P < 0.06). The amount of Feeding time did not differ for the two groups. Time allocated to each maternal behavior Comparison o f amount o f time allocated to maternal behaviors f o r the two groups. Table II presents the results of analyses comparing the means of the ten maternal behaviors for the premature and fullterm infants. Four maternal variables exhibited significant differences between the groups. Over the total 7-h day, mothers of prematures moved their infants less often (F(1, 35) = 6.43, P < 0.05), talked to their infants less (F(1, 35) = 5.23, P < 0.05), looked at their infants less often (F(1, 35) = 5.73, P < 0.05), and held their infants less (F(1, 35) = 6.62, P < 0.05).
227 TABLE II Over the 4-weekly observations, the mean percent of the 7-h day spent in each context and social behavior by the mothers of the premature and fullterm infants. Significance levels of individual difference analyses are indicated by asterisks, and variables differing significantly between prematures and fullterms are underlined. For individual differences analyses: * P < 0.10; * * P < 0.05; ***P< 0.01; ****P< 0.001.
lnteractional Contexts Feeding Change or Bathe a
Social Contact Baby Alone ~ Maternal Behaviors Move ~
Rock Pat Caress Talk R Look a Vis-a-Vis Hold or Carry ~ Smile or Laugh Suck Stimulate
Prematures
Fullterms
Mean 070(S.D.)
Mean % (S.D.)
12.6 (5.8)*** 1.9 (0.8)* 8.5 (3.5) 76.9 (6.8)**
15.8 (6.3)**** 2.8 (1.0)** 14.1 (8.2)**** 67.2 (11.0)****
4.1 (1.3)***
5.9 (2.0)****
3.4 (2.8) 3.0 (1.5)** 5.9 (3.7)**** 5.4 (3.4)**** 18.6 (6.4)*** 1.5 (0.9)* 18.2 (7.2)**** 0.7 (1.2)**** 1.4 (1.2)***
7.1 (7.9)**** 3.8 (2.2)**** 7.6 (3.4)**** 9.6 (5.1)**** 26.0 (9.1)**** 2.1 (1.1)*** 27.5 (10.I)**** 1.2 (0.8)**** 1.4 (1.2)****
Rp< 0.05 for differences between prematures and fullterms.
Changes in the amount o f maternal behaviors over time. Two maternal variables exhibited a significant increase over weeks for both premature and fuUterm infants: Vis-a-Vis (F(3, 101) = 4.09, P < 0.01) and Smile or Laugh (F(3, 101) = 2.90, P <
0.05). Comparison o f maternal stimulation levels when the infants are with their mothers Several studies have found that mothers o f premature infants are more active in initiating and maintaining interactions [3,4,20]. It is possible, therefore, that the lower amount o f maternal stimulation received by our premature infants was due to the lower amount o f time they spent with their mothers and that during this time their mothers were actually more active than the mothers o f fullterms. To test for this possibility, we measured the ten maternal variables as percentages o f the time the infants were in physical contact with their mothers and compared the groups with analyses of variance. There were no significant differences between the groups in the amount o f any maternal behavior. As Table III indicates, the means for the groups were generally very close and, for six o f ten variables, lower for the mothers o f prematures. Thus, there is no evidence that mothers o f prematures are more active during interactions than mothers o f fullterms.
228 T A B L E III Mean and standard deviation o f each maternal behavior measured as a percent o f the time the infant is in physical contact with the mother. Prematures
Move Rock Pat Caress Talk Look Vis-a-Vis Hold or Carry Smile or L a u g h Suck Stimulate
Fullterms
Mean
S.D.
Mean
S.D.
17.9 9.2 11.9 23.9 20.8 72.5 6.5 77.6 2.8 5.9
2.6 8.4 3.0 9.8 10.4 11.0 2.7 13.8 3.9 4.6
18.7 18.2 11.9 23.7 28.1 74.1 6.0 82.5 3.5 4.5
4.5 15.5 6.3 6.7 12.2 12.2 3.5 5.1 2.8 4.0
The effects o f birth order, sex and neonatal complications The premature infants formed a heterogeneous group that differed from each other and the fullterms on a number of demographic variables, including birth order, sex, birth weight, obstetrical complications, and neonatal complications. Three of these, birth order, sex, and neonatal complications, were chosen for further analysis because of their potential effect on maternal behaviors. Effect o f birth order on the group differences. Since the birth order of the infant might have different effects on the behaviors of the mothers of premature and fullterm infants, the effects of birth order were included in each analysis. There were no significant interactions between Birth Order and Group for any variable, either interactional context or maternal behavior. In addition, there were no significant interactions between Birth Order and Week. Effect o f sex on the group differences. The premature group had a slightly lower proportion of male infants than the fullterm group (50°70 vs. 59070). Since mothers may behave differently to male and female infants, some of the differences in the maternal behaviors for the premature and fullterm infants might be explained by the different proportions of males and females in the two groups. To explore this possibility, the main effect for Sex in the individual differences analyses of the four interactional contexts and the ten maternal behaviors was examined. None of the variables that had shown a significant difference between the two groups of infants had a main effect for Sex that approached significance at the 0.10 level for either prematures or fullterms. Thus, the different percentage of males and females in the two groups of infants cannot be a major factor in the maternal behavioral differences between the groups. Effects o f neonatal complications on group differences. Since some researchers have indicated that mothers provide less stimulation to sick premature infants than healthier prematures [17,36], it is possible that our results reflect, in part, the pres-
229 ence of sick prematures in our sample. To check for this possibility, correlations between the number of neonatal complications, as measured on the Postnatal Complications Scale [32], and the amount of each interactional context and maternal behavior were calculated for the group of premature infants. In all cases, the relationship between neonatal complications and the maternal variables was small and did not reach a 0.20 probability level. Thus, the sub-group of sick premature infants cannot be the major source of the differences found between the mothers of prematures and fullterms. Discussion
It is clear that, throughout the early post-term weeks of life, the social environment of premature infants differs from that of fullterms. Over the 7-h day in the home, premature infants experience significantly less maternal stimulation. Mothers of prematures spent much less time with their infants (left them alone more) than mothers of fullterms. Concomitantly, mothers spent less time looking at, moving, talking to, and holding premature infants. In fact, the prematures did not experience more of any maternal behavior than fullterms. This lower amount of maternal stimulation is even more dramatic in view of our finding from an earlier study that premature infants are awake and alert more than fullterms when they are with their mothers and when they are alone [15]. This general finding of less maternal stimulation for the prematures is in disagreement with the findings of some previous studies that mothers of prematures are more active in interactions than mothers of fullterms [3,4,20]. These studies were based on observations of mothers and their premature infants interacting in the laboratory, using brief observations and a prescribed situation; whereas, the two studies that used home observations agree with us in finding either less maternal stimulation for premature infants [48] or no differences between premature and fullterm infants [28]. Our findings are also consistent with the results of studies that have reported lower levels of specific maternal behaviors for premature infants [5,14,17,30]. However, our findings indicate that the primary way that mothers provide lower amounts of stimulation is by reducing physical contact with the premature infant, rather than by being less stimulating while they are interacting. The systematic nature of the differences between mothers of prematures and full terms highlights commonalities among prematures in their early social environment, despite the differences among them. Any group of prematures is likely to be heterogeneous, and this one was not an exception. For example, the gestational ages at birth of the premature infants ranged from 28 to 35 weeks, and their medical courses varied from essentially no problems to complications requiring intensive care and mechanical ventilation. Yet, despite this variability, differences between the two groups were still found to be significant. Clearly, there are similarities in the early social experiences of premature infants despite their heterogeneity. The finding that the social environment of premature infants is characterized by lower levels of maternal stimulation than fullterm infants should have implications for later development of these infants. Studies of both premature and fullterm
230
infants have shown that the quality of maternal attention is related to developmental outcome [7,8,10,11,13]. Premature infants are generally described as having poorer developmental outcomes than fullterm infants [12,26,39,41]. It might be expected that these findings are related. For example, the lower amount of maternal vocalizations the prematures may be related to their later language abilities. Prematures are known to show language delays at age 2 [25,47], and studies have shown that language ability is related to maternal verbal stimulation and responsiveness [6,34]. Nevertheless, it is reasonable to speculate that lower levels of maternal stimulation may be appropriate for premature infants during the early post-term weeks. That is, the needs of prematures for social stimulation may differ from those of fullterms. First, the neurobehavioral organization of premature infants is different from that of fullterms. This is expressed most directly in markedly different patterns of sleep and waking states during the early post-term weeks [15,37,43]. Second, prematures differ from fullterm infants in being generally more sensitive to stimulation. This increased sensitivity is present prior to term and continues into the post-term period [2,9,33]. Accordingly, prematures respond more positively to maternal stimulation when its intensity is reduced [20,22]. Thus, it is possible that the mothers of these infants were responding to their infants' behaviors when they left them alone more and stimulated them less. For example, premature infants cry less when they are with their mothers than fullterms [15]. Thus, they may demand less maternal attention. However, lower levels of social stimulation for prematures may not continue to be appropriate as the infants become older. It is possible that mothers of premature infants, accustomed to providing less stimulation in the early weeks after term, may not increase their contact appropriately in later months to provide adequate stimulation for language and social development. Clearly, determining the optimal social experience for the development of premature infants and providing this experience will be a complex task, both for researchers and for parents.
Acknowledgements We wish to thank Victor H. Denenberg for statistical consultation and Mark C. Davis for programming assistance. The preparation of this paper was supported by Grant No. MH-41244 from the National Institute of Mental Health, Center for Prevention Research, division of Prevention and Special Mental Health Programs.
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mother-infant interactions. In: Infant behavior and development: Perinatal risk and newborn behavior, pp. 139--152. Editors: L.P. Lipsitt and T.M. Field. Ablex, Norwood, NJ. Lawson, K., Daum, C. and Turkewitz, G. (1977): Environmental characteristics of a neonatal intensive care unit. Child Dev., 48, 1633--1639. Leifer, A.D., Leiderman, P.H., Barnett, C.R. and Williams, J.A. (1972): Effects of mother-infant separation on maternal attachment behavior. Child Dev., 43, 1203--1218. Lester, B.M., Hoffman, J. and Brazelton, T.B. (1985): The rhythmic structure of mothr-infant interaction in term and preterm infants. Child Dev., 56, 15--27. Littman, B. and Parmeiee, A.H. (1978): Medical correlates of infant development. Pediatrics, 61, 470--474. McGehee, L.J. and Eckerman, C.O. (1983): The preterm infant as a social partner: Responsive but unreadable. Infant Behav. Dev., 6, 467--470. Metzl, M.N. (1980): Teaching parents a strategy for enhancing infant development. Child Dev., 51, 583--586. Minde, K., Ford, L., Celhoffer, L. and Boukydis, C. (1975): Interactions of mothers and nurses with premature infants. Can. Med. Assoc. J., 113, 741--745. Minde, K., Whitelaw, A., Brown, J. and Fitzhardinge, P. (1983): Effect of neonatal complications in premature infants on early parent-infant interactions. Dev. Med. Child Neurol., 25,763--777. Parmelee, A.H. (1975): Neurophysiological and behavioral organization of premature infants in the first months of life. Biol. Psychiatry, 10, 501--511. Prechtl, H.F.R. (1968): Neurological findings in newborn infants after pre- and postnatal complications. In: Aspects of prematurity and dysmaturity: Proceedings of Nutricia Symposium, 1967, pp. 303. Editors: J.H.P. Jonxis, H.K.A. Visser and J.A. Troelstra. Stenfert Kroese NV, Leiden. Saigal, S., Rosenbaum, P., Stoskopf, B. and Milner, R. (1982): Follow-up of infants 501 to 1,500 gm birth weight delivered to residents of a geographically defined region with perinatal intensive care facilities. J. Pediatr., 100, 606--613. Sameroff, A.J. and Chandler, M.J. (1975): Reproductive risk and the continuum of caretaking casualty. In: Review of child development research, Vol. 4, pp 187--244. Editor: F.D. Horowitz. University of Chicago Press, Chicago. Siegel, L.S. (1983): Correction for prematurity and its consequences for the assessment of the very low birth weight infant. Child Dev., 54, 1176--1188. Thoman, E.B. (1980): Disruption and asynchrony in early parent-infant inteactions. In: Exceptional infant: Psychosocial risks in infant-environment transactions, Vol. 4, pp 91--119. Editors: D.B. Sawin, R.C. Hawkins II, L.O. Walker and J.H. Penticuff. Brunner/Mazel, New York. Thoman, E.B. (1982): A biological perspective and a behavioral model for assessment of premature infants. In: Primary prevention of psychopathology: Facilitating infant and early childhood development, Vol. 6, pp. 159--179. Editors: L.A. Bond and J.M. Joffee. University Press of New England, Hanover, NH. Thoman, E.B., Acebo, C. and Becker, P.T. (1983): Infant crying and stability in the mother-infant relationship: A systems analysis. Child Dev., 54,653--659. Thoman, E.B., Acebo, C., Dreyer, C.A., Becker, P.T. and Freese, M.P. (1979): Individuality in the interactive process. In: Origins of the infant's social responsiveness, pp. 305--338. Editor: E.B. Thoman. Lawrence Erlbaum, Hillsdale, NJ. Thoman, E.B., Becker, P.T. and Freese, M.P. (1978): Individual patterns of mother-infant interaction. In: Observing behavior: Theory and applications in mental retardation, Vol. 1, pp. 95--t14. Editor: G.P. Sackett. University Park Press, Baltimore. Ungerer, J.A. and Sigman, M. (1983): Developmental lags in preterm infants from one to three years of age. Child Dev., 54, 1217--1228. Watt, J. and Strongman, K.T. (1985): Mother-infant interactions at 2 and 3 months in preterm, small-for-gestational-age, and full-term infants; their relationship with cognitive development at 4 months. Early Hum. Dev., 11, 231--246. Winer, B. (1971): Statistical principles in experimental design, 2nd edn. McGraw-Hill, New York.
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Elsevier Scientific Publishers Ireland Ltd. EHD 00904
The early social environment of premature and fullterm infants D i a n e H o l d i t c h D a v i s a n d E v e l y n B. T h o m a n Department o f Biobehavioral Sciences, The University of Connecticut, Storrs, CT 06268, U.S.A. Accepted for publication 12 November 1987
Summary The behaviors of 10 mothers of prematures and 29 mothers of fullterms were compared from 7-h observations made in the home when the infants were 2, 3, 4 and 5 weeks post-term. The observation day was divided into four mutually exclusive interactional contexts that together made up the total day: feeding time, changing or bathing time, time when the mother and infant were in physical contact but the mother was not caretaking, and time the infant was alone. Measures of ten maternal behaviors were also compared: moving, rocking, patting, caressing, talking, looking, engaging in vis-a-vis with the baby, holding or carrying, smiling or laughing, and stimulating the baby to suck. Mothers of prematures left their infants alone more and changed them less than mothers of fullterms. In addition, mothers of prematures moved their infants less often, talked to their infants less, looked at their infants less, and held their infants less. These results indicate that, over the 7-h day, prematures receive markedly less stimulation than fullterms. Since the neurobehavioral characteristics of premature and fullterm infants are known to differ [15], it is suggested that these differences in maternal behaviors may be in response to infant cues and appropriate for the infants. premature infants; infants; mothers; mother-infant interaction; social environment
Introdution The role of the social environment in the development of premature infants has received considerable attention [7,13,40]. Studies indicate that it may be an important factor in the developmental course of these vulnerable infants. For Address for correspondence: Diane Holditch Davis, School of Nursing, CB No. 7460 Carrington Hall, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599-7460, U.S.A. 0378-3782/88/$03.50 © 1988 Elsevier Scientific Publishers Ireland Ltd. Published and Printed in Ireland
222 example, Sameroff and Chandler reported that infant outcome is more directly related to the social environment than to adverse perinatal experiences [40]. Cohen and Beckwith have suggested that optimal maternal stimulation may be able to ameliorate the effects of perinatal stresses; whereas, inappropriate stimulation may actually worsen these effects [13]. A number of recent studies have explored the early hospital environment of premature infants and, in particular, the types of stimulation they receive from their caregivers in the hospital [19,23,24,29,35]. However, the home environment of prematures in the first few months after hospital discharge and the stimulation they receive from caregivers in the home has received less attention. Interactions between prematures and their mothers during this early post-term period have most often been studied in the laboratory, an environment that might alter the nature of the interaction; and the few studies conducted in the home have generally been limited to a single interactional situation. Yet, behaviors in a single situation may not be typical of the whole relationship. With these variations in social situation, it is not surprising that the results of studies of the early behaviors of mothers of prematures have been contradictory. Some reports indicate that mothers of prematures display less positive affect toward the infant [14,17,21,30] and less synchrony in their interactions [27,31]. Other studies have found that mothers of prematures cuddle their infants less [30], talk to their infants less [4,5,17], and touch their infants less [3,14,17,30]. Still other studies have found that mothers of premature infants are more active in initiating and maintaining interactions [3,4,20]. In still other studies, the behaviors of mothers of prematures have been found not to differ from those of mothers of fullterms in the early weeks after term [1,28]. Thus, generalizations about the nature of premature mothering are still difficult. The purpose of this study was to describe the early social environment of premature infants, including the types of stimulation they receive from their mothers, over the range of circumstances that typically occur in the home. These social experiences of prematures were compared with those of healthy fullterm infants. Prolonged, naturalistic observations were made in the home when the infants were 2, 3, 4 and 5 weeks post-term, and the maternal behaviors were observed for a 7-h period each week. The way the mothers allocated their time to different social situations was determined by dividing the 7-h day into four mutually exclusive interactional contexts: Feeding, Change or Bathe, Social Contact, and Baby Alone. These interactional contexts were chosen because a previous study of fuUterm infants had indicated that they reliably discriminate among individuals and show predictive validity [44]. Measures of ten specific maternal behaviors were also examined. Methods
Subjects The subjects for this study were 10 premature infants and 29 fullterm infants who were enrolled in the Connecticut Longitudinal Project, a research study that
223 was approved by the institutional review boards of all participating hospitals [42,45,46]. Subjects, both premature and fullterm, were selected based on their availability at the time the laboratory was free to enroll a new subject and the willingness of the mother to be involved in the study. Mothers of both groups of infants gave informed consent for the study prior to their infant's discharge from the hospital. Fullterm subjects were recruited during the last month of pregnancy or during the postnatal hospitalization period. The only criterion for the selection of fullterm infants was that they have uncomplicated perinatal courses. The premature infants were enrolled during the preterm period after their medical conditions had stabilized. The selection criteria for these infants were that they were born at least 4 weeks prior to their obstetrical due dates and would be discharged home by 1 week post-term so that they would be available for home observations at the same post-term ages as the fullterms. (In actuality, all of the prematures in this study were discharged home before their term date.) The prematures had experienced a wide variety of medical courses, ranging from no complications and discharge home in the first week to respiratory distress syndrome and mechanical ventilation, but all were judged by pediatric examination to be healthy premature infants by the time of hospital discharge. These criteria were chosen so that a heterogeneous group of premature infants, representative of the vast majority of prematures who leave the hospital without obvious disabilities would be studied. Infants in both groups were Caucasian, single births, and average weight for gestational age. Five of the premature infants and 12 of the fullterms were secondborn and had an older fullterm sibling. The fullterm infants were discharged within 5 days after birth, and all prematures were discharged prior to their estimated term dates (mean 25 days). The parents of both groups were married, lived in single family homes, and were of lower middle to middle income levels. The infants were cared for primarily by their mothers with the exception of one premature infant who was cared for by a grandmother during the day. The demographic characteristics of the two groups of infants are given in Table I. The gestational ages of the infants were calculated from the obstetric estimated date of confinement which had been determined from either the date of the mother's last menstrual period of from ultrasound examinations. All of the gestational ages agreed within 2 weeks with the results of Dubowitz examinations [18] performed within 48 h of birth, and all fullterm infants had scores within 2 weeks of 40 weeks gestational age.
Procedures for observations This report is based on 7-h observations made in the home from approx. 0900 h to 1600 h when the infants were 2, 3, 4 and 5 weeks post-term. The mothers were familiar with the observational procedures because they and their infants had been observed together prior to the first observation in the present study. Mother and infant behaviors were recorded on a code sheet every 10 s throughout the observation. The end of each 10-s epoch was signaled through an ear phone from a small electronic timing device. At this signal, the observer wrote the codes for all variables
224 TABLE I Demographic characteristics of the premature and fuUterm infants. Prematures Mean Males/females First-/second-born Gestational age (weeks) Birth weight (g) Maternal age (years) Obstetric complicationsa Vaginal delivery/cesarean section l-rain Apgar 5-rain Apgar Neonatal complicationsb
5/5 5/5 31 1520 26 8.5 5/5 6.2 7.7 2.5
Fullterms Range
28--35 1260--2100 16--33 3-- 11 2--10 6--10 0--6
Mean 17/12 17/12 40 3536 26 3.1 28/1 8.9 9.7 0.2
Range
37--42 2750--4395 21 --34 2--6 7--10 9--10 0-- 1
aScored on Prechtl Scale [38]. Possible number of non-optimal events ranges from 0 to 42. bScored on Postnatal Complications Form [321. Possible number of non-optimal events ranges from 0 to 10.
occurring during the epoch on a sheet of paper. The observer remained in the room with the infant throughout the 7-h day recording maternal and infant behaviors. Each observation was shared by two observers, each recording for approx. 3.75 h. The changing of observers in the middle of the observation was accomplished without interruption of either the observational procedures or the ongoing household activities. The two observers recorded for a 15-rain overlap period so that ongoing reliability could be assessed. Inter-rater reliability for each variable was calculated for all observers on an ongoing basis, using this formula: 2 x number of epochs with agreements number of epochs recorded by observer 1 + observer 2 A minimum overall agreement of 85 % was maintained. Variables used f o r data analyses Interactional contexts. The observation was divided into four mutually exclusive interactional contexts which together made up the total observation day: (i) Feeding
the mother is either feeding the baby by breast, bottle, or spoon or is pausing briefly (< 10 rain) in the middle of a feeding, as for burping. (ii) C h a n g e or B a t h e - the mother is changing or bathing the baby. (iii) Social Contact ~ the mother is in physical contact with the baby (i.e., holding or touching) but is not feeding, changing, or bathing. (iv) B a b y A l o n e ~ the infant is not being held or touched by the mother.
225 M a t e r n a l b e h a v i o r s . Ten social behaviors were recorded in any epoch in which they occurred. Multiple occurrences of the same behavior in the same epoch were not recorded. These variables were defined as follows: (i) M o v e ~ The mother moves the baby so as to change the baby's position in space. (ii) R o c k - - the mother rocks the baby for at least two cycles. (iii) P a t - - The mother pats the baby. (iv) C a r e s s ~ The mother touches the baby in a light, non-rhythmic manner, such as strokes, kisses, nuzzles, wipes, tickles, and hand holding. (v) T a l k - - The mother talks to the infant. (vi) L o o k ~ The mother looks at the infant. (vii) Vis-a-Iris The mother and baby look at each other and have eye to eye contact. (viii) H o l d o r C a r r y ~ The mother is holding or carrying the infant. (ix) S m i l e o r L a u g h ~ The mother smiles or laughs at the baby. (x) S u c k S t i m u l a t e - - The mother moves the breast, bottle, pacifier, or her finger to elicit sucking. The stimulation provided on rare occasions by caregivers other than the mother was included in the maternal behaviors analyzed, as the focus of this study was the social experiences of the infants. Measures o f variables
The four interactional context and the ten maternal behaviors were each measured as a percentage of the total observation time. Each maternal behavior was also measured as a percentage of the time the infants were in physical contact with their mother (i.e. during Feeding, Change or Bath, and Social Contact). Statistical analyses
One fullterm and three premature infants were each missing one observation. The missing values were estimated using the procedure described in Winer [49, see pp. 487--488]. these estimates were used in all of the analyses described in this paper. The degrees of freedom were appropriately reduced to compensate for these estimations. I n d i v i d u a l d i f f e r e n c e s . Individual differences for the interactional contexts and the maternal variables were assessed separately for the fullterm and premature infants using a two-factor repeated measures analysis of variance for each variable. The ANOVA included the following sources of variance: Sex, Subjects, Weeks, Sex by Weeks, and Subjects by Weeks. To test for individual differences, the Mean Square for Subjects was divided by the Mean Square for Subjects by Weeks with the assumption that Weeks is a random variable [16,49]. G r o u p c o m p a r i s o n s . The percentage of the total observation that the mothers of the prematures and fullterms spent in each of the interactional contexts and in each maternal behavior was compared by using a repeated measures analysis of variance for each variable. Three-factor (Group by Birth Order by Week) ANOVAs were used for the interactional contexts, and four-factor (Group by Birth Order by Context by Week) ANOVAs for the social behaviors. In addition, each maternal behavior was measured as a percentage of the time the infants were in physical contact with their mothers. The two groups of infants were compared using three-factor (Group by Birth Order by Week) repeated measures ANOVA for each of these variables. The Birth Order factor was included in each of these analyses to account for
226 the possibility that mothers of premature and fullterm infants might respond differently as a function of the infant's birth order. Because of the difference in the sample size of the two groups, each analysis of variance used an unweighted means procedure, thereby giving equal weight to the means of the two groups rather than giving greater weight to the group with the larger sample size. Since the variances of five of the ten maternal variables and two of the interactional contexts were significantly greater for the fullterms than for the premature infants, the mean differences were also calculated using (i) the Mann-Whitney non-parametric test and (ii) a conservative F-test using the larger variance for the error term with its associated degrees of freedom. In all instances in which the primary analysis found significant main effects, these tests also found significance. Relation between neonatal complications and maternal behaviors. To determine whether the amount of neonatal complications affects the maternal behaviors of premature infants, correlations between the number of neonatal complications, as measured on the Postnatal Complications Scale [32], and the amount of each interactional context and maternal behavior were calculated for the group of premature infants. Results
Individual differences Table II presents the results of the individual differences analyses for the fullterm and premature infants. Significant individual differences were found for the amounts of time allocated to each variable for the fullterms. Despite the smaller number of subjects in the premature group, two of the interactional contexts and eight of the maternal behaviors exhibited significant individual differences. Two other variables approached significance. Time spent in each context by the prematures and fullterms Table II also presents the amounts of the interactional contexts averaged over the 4 weeks for the two groups of infants and the results of analyses comparing the amounts of these variables for premature and fullterm infants. The premature infants spent significantly more time in Baby Alone than the fullterms (F(1, 35) = 6.39, P < 0.05) and significantly less time in Change or Bathe (F(1, 35) = 6.70, P < 0.05). The lesser amount of Social Contact for the prematures approached significance (F(I, 35) = 3.79, P < 0.06). The amount of Feeding time did not differ for the two groups. Time allocated to each maternal behavior Comparison o f amount o f time allocated to maternal behaviors f o r the two groups. Table II presents the results of analyses comparing the means of the ten maternal behaviors for the premature and fullterm infants. Four maternal variables exhibited significant differences between the groups. Over the total 7-h day, mothers of prematures moved their infants less often (F(1, 35) = 6.43, P < 0.05), talked to their infants less (F(1, 35) = 5.23, P < 0.05), looked at their infants less often (F(1, 35) = 5.73, P < 0.05), and held their infants less (F(1, 35) = 6.62, P < 0.05).
227 TABLE II Over the 4-weekly observations, the mean percent of the 7-h day spent in each context and social behavior by the mothers of the premature and fullterm infants. Significance levels of individual difference analyses are indicated by asterisks, and variables differing significantly between prematures and fullterms are underlined. For individual differences analyses: * P < 0.10; * * P < 0.05; ***P< 0.01; ****P< 0.001.
lnteractional Contexts Feeding Change or Bathe a
Social Contact Baby Alone ~ Maternal Behaviors Move ~
Rock Pat Caress Talk R Look a Vis-a-Vis Hold or Carry ~ Smile or Laugh Suck Stimulate
Prematures
Fullterms
Mean 070(S.D.)
Mean % (S.D.)
12.6 (5.8)*** 1.9 (0.8)* 8.5 (3.5) 76.9 (6.8)**
15.8 (6.3)**** 2.8 (1.0)** 14.1 (8.2)**** 67.2 (11.0)****
4.1 (1.3)***
5.9 (2.0)****
3.4 (2.8) 3.0 (1.5)** 5.9 (3.7)**** 5.4 (3.4)**** 18.6 (6.4)*** 1.5 (0.9)* 18.2 (7.2)**** 0.7 (1.2)**** 1.4 (1.2)***
7.1 (7.9)**** 3.8 (2.2)**** 7.6 (3.4)**** 9.6 (5.1)**** 26.0 (9.1)**** 2.1 (1.1)*** 27.5 (10.I)**** 1.2 (0.8)**** 1.4 (1.2)****
Rp< 0.05 for differences between prematures and fullterms.
Changes in the amount o f maternal behaviors over time. Two maternal variables exhibited a significant increase over weeks for both premature and fuUterm infants: Vis-a-Vis (F(3, 101) = 4.09, P < 0.01) and Smile or Laugh (F(3, 101) = 2.90, P <
0.05). Comparison o f maternal stimulation levels when the infants are with their mothers Several studies have found that mothers o f premature infants are more active in initiating and maintaining interactions [3,4,20]. It is possible, therefore, that the lower amount o f maternal stimulation received by our premature infants was due to the lower amount o f time they spent with their mothers and that during this time their mothers were actually more active than the mothers o f fullterms. To test for this possibility, we measured the ten maternal variables as percentages o f the time the infants were in physical contact with their mothers and compared the groups with analyses of variance. There were no significant differences between the groups in the amount o f any maternal behavior. As Table III indicates, the means for the groups were generally very close and, for six o f ten variables, lower for the mothers o f prematures. Thus, there is no evidence that mothers o f prematures are more active during interactions than mothers o f fullterms.
228 T A B L E III Mean and standard deviation o f each maternal behavior measured as a percent o f the time the infant is in physical contact with the mother. Prematures
Move Rock Pat Caress Talk Look Vis-a-Vis Hold or Carry Smile or L a u g h Suck Stimulate
Fullterms
Mean
S.D.
Mean
S.D.
17.9 9.2 11.9 23.9 20.8 72.5 6.5 77.6 2.8 5.9
2.6 8.4 3.0 9.8 10.4 11.0 2.7 13.8 3.9 4.6
18.7 18.2 11.9 23.7 28.1 74.1 6.0 82.5 3.5 4.5
4.5 15.5 6.3 6.7 12.2 12.2 3.5 5.1 2.8 4.0
The effects o f birth order, sex and neonatal complications The premature infants formed a heterogeneous group that differed from each other and the fullterms on a number of demographic variables, including birth order, sex, birth weight, obstetrical complications, and neonatal complications. Three of these, birth order, sex, and neonatal complications, were chosen for further analysis because of their potential effect on maternal behaviors. Effect o f birth order on the group differences. Since the birth order of the infant might have different effects on the behaviors of the mothers of premature and fullterm infants, the effects of birth order were included in each analysis. There were no significant interactions between Birth Order and Group for any variable, either interactional context or maternal behavior. In addition, there were no significant interactions between Birth Order and Week. Effect o f sex on the group differences. The premature group had a slightly lower proportion of male infants than the fullterm group (50°70 vs. 59070). Since mothers may behave differently to male and female infants, some of the differences in the maternal behaviors for the premature and fullterm infants might be explained by the different proportions of males and females in the two groups. To explore this possibility, the main effect for Sex in the individual differences analyses of the four interactional contexts and the ten maternal behaviors was examined. None of the variables that had shown a significant difference between the two groups of infants had a main effect for Sex that approached significance at the 0.10 level for either prematures or fullterms. Thus, the different percentage of males and females in the two groups of infants cannot be a major factor in the maternal behavioral differences between the groups. Effects o f neonatal complications on group differences. Since some researchers have indicated that mothers provide less stimulation to sick premature infants than healthier prematures [17,36], it is possible that our results reflect, in part, the pres-
229 ence of sick prematures in our sample. To check for this possibility, correlations between the number of neonatal complications, as measured on the Postnatal Complications Scale [32], and the amount of each interactional context and maternal behavior were calculated for the group of premature infants. In all cases, the relationship between neonatal complications and the maternal variables was small and did not reach a 0.20 probability level. Thus, the sub-group of sick premature infants cannot be the major source of the differences found between the mothers of prematures and fullterms. Discussion
It is clear that, throughout the early post-term weeks of life, the social environment of premature infants differs from that of fullterms. Over the 7-h day in the home, premature infants experience significantly less maternal stimulation. Mothers of prematures spent much less time with their infants (left them alone more) than mothers of fullterms. Concomitantly, mothers spent less time looking at, moving, talking to, and holding premature infants. In fact, the prematures did not experience more of any maternal behavior than fullterms. This lower amount of maternal stimulation is even more dramatic in view of our finding from an earlier study that premature infants are awake and alert more than fullterms when they are with their mothers and when they are alone [15]. This general finding of less maternal stimulation for the prematures is in disagreement with the findings of some previous studies that mothers of prematures are more active in interactions than mothers of fullterms [3,4,20]. These studies were based on observations of mothers and their premature infants interacting in the laboratory, using brief observations and a prescribed situation; whereas, the two studies that used home observations agree with us in finding either less maternal stimulation for premature infants [48] or no differences between premature and fullterm infants [28]. Our findings are also consistent with the results of studies that have reported lower levels of specific maternal behaviors for premature infants [5,14,17,30]. However, our findings indicate that the primary way that mothers provide lower amounts of stimulation is by reducing physical contact with the premature infant, rather than by being less stimulating while they are interacting. The systematic nature of the differences between mothers of prematures and full terms highlights commonalities among prematures in their early social environment, despite the differences among them. Any group of prematures is likely to be heterogeneous, and this one was not an exception. For example, the gestational ages at birth of the premature infants ranged from 28 to 35 weeks, and their medical courses varied from essentially no problems to complications requiring intensive care and mechanical ventilation. Yet, despite this variability, differences between the two groups were still found to be significant. Clearly, there are similarities in the early social experiences of premature infants despite their heterogeneity. The finding that the social environment of premature infants is characterized by lower levels of maternal stimulation than fullterm infants should have implications for later development of these infants. Studies of both premature and fullterm
230
infants have shown that the quality of maternal attention is related to developmental outcome [7,8,10,11,13]. Premature infants are generally described as having poorer developmental outcomes than fullterm infants [12,26,39,41]. It might be expected that these findings are related. For example, the lower amount of maternal vocalizations the prematures may be related to their later language abilities. Prematures are known to show language delays at age 2 [25,47], and studies have shown that language ability is related to maternal verbal stimulation and responsiveness [6,34]. Nevertheless, it is reasonable to speculate that lower levels of maternal stimulation may be appropriate for premature infants during the early post-term weeks. That is, the needs of prematures for social stimulation may differ from those of fullterms. First, the neurobehavioral organization of premature infants is different from that of fullterms. This is expressed most directly in markedly different patterns of sleep and waking states during the early post-term weeks [15,37,43]. Second, prematures differ from fullterm infants in being generally more sensitive to stimulation. This increased sensitivity is present prior to term and continues into the post-term period [2,9,33]. Accordingly, prematures respond more positively to maternal stimulation when its intensity is reduced [20,22]. Thus, it is possible that the mothers of these infants were responding to their infants' behaviors when they left them alone more and stimulated them less. For example, premature infants cry less when they are with their mothers than fullterms [15]. Thus, they may demand less maternal attention. However, lower levels of social stimulation for prematures may not continue to be appropriate as the infants become older. It is possible that mothers of premature infants, accustomed to providing less stimulation in the early weeks after term, may not increase their contact appropriately in later months to provide adequate stimulation for language and social development. Clearly, determining the optimal social experience for the development of premature infants and providing this experience will be a complex task, both for researchers and for parents.
Acknowledgements We wish to thank Victor H. Denenberg for statistical consultation and Mark C. Davis for programming assistance. The preparation of this paper was supported by Grant No. MH-41244 from the National Institute of Mental Health, Center for Prevention Research, division of Prevention and Special Mental Health Programs.
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