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Journal of Pediatric Psychology, Vol. 28, No. 8, 2003, pp. 529-534
© 2003 Society of Pediatric Psychology

Brief Report: Breast-fed One-Week-Olds Demonstrate Superior Neurobehavioral Organization

Sybil Hart, PhD1, L. Mallory Boylan, PhD1, Sebrina Carroll, MS1, Yvette A. Musick, MS1 and Richard M. Lampe, MD2

1 Texas Tech University, Department of Pediatrics, 2 Texas Tech University Health Sciences Center, Department of Pediatrics

All correspondence concerning this article should be addressed to Dr. Sybil Hart, Texas Tech University, Department of Human Development and Family Studies, Lubbock, Texas 79409-1162. E-mail: sybil.hart{at}ttu.edu.


    Abstract
 Top
 Abstract
 Introduction
 Method
 Results
 Discussion
 References
 
Objectives Following studies conducted during the immediate newborn stage, we investigated whether one-week-olds' neurobehavioral functioning was differentiated by feeding method. We also examined whether feeding-method effects differed among infants of adolescent mothers. Method Participants were infants (N = 83) of breast-feeding (N = 41) and formula-feeding (N = 42) mothers. Approximately half of each group's participants had adolescent mothers and half were infants of adult mothers. Assessments on the Brazelton Neonatal Behavioral Assessment Scale (BNBAS) were conducted on the infants when they were 8.95 days of age. Results Breast-fed infants surpassed formula-fed infants on items of the orientation, motor, range of state, and state regulation dimensions of the BNBAS. Breast-fed infants also exhibited fewer abnormal reflexes, signs of depression, and withdrawal. Infants of adolescent mothers did not differ from those of adult mothers, regardless of feeding method. Conclusion These data provide compelling evidence that breast-feeding is advantageous to neonates' neurobehavioral organization.

Key words: breast-feeding; adolescent mothers; neonates; BNBAS.


    Introduction
 Top
 Abstract
 Introduction
 Method
 Results
 Discussion
 References
 
Advantages of breast-feeding to infants' physiological and immune functioning are well documented, yet findings on benefits to infant behavior have been equivocal. Since the attachment process is facilitated by optimized infant behavior (Brazelton & Nugent, 1995Go; Hart, Field, & Nearing, 1998Go), this issue warrants clarification. Research using neonates is particularly informative, since differences at the newborn stage are less attributable to confounding factors stemming from self-selection, such as socioeconomic status (SES). Early works which often identified crying and fussiness in breast-fed neonates were followed by a large-scale study by DiPietro, Larson, and Porges (1987Go). During administration of the Brazelton Neonatal Behavioral Assessment Scale (BNBAS; Brazelton & Nugent, 1995Go), these infants were found to be more irritable, less able to regulate behavioral state, less consolable, and more demanding of examiner efforts to maintain proper arousal. A difficulty with that study, however, was its reliance on data collected only 37 hours after delivery, opening the possibility that having had only minimal exposure to colostrum, breast-fed infants' greater fussiness may have stemmed simply from hunger. DiPietro and associates refuted this point, citing breast-fed infants' slower heart rate as evidence of decreased arousal, which they considered incompatible with hunger. Nevertheless, it is clear that weight loss during the immediate postpartum period is greater among breast-fed infants (Dollberg, Lahav, & Mimouni, 2001Go), suggesting that hunger cannot be ruled out as a potential confound.

Behavioral differences between breast- and formula-fed neonates may be evaluated with greater validity by examining newborn behavior a few days after delivery, when lactation is more likely to have been initiated but still prior to the establishment of a substantiative interaction history. Using 7-day-olds, Bernal (1972Go) found greater crying in breast-fed infants. Again implicating the influence of hunger, however, the investigator noted that mothers had been advised to conduct feedings on a strict 4-hour schedule, and by adhering to this regimen, breast-feeding mothers were encountering problems establishing lactation and greater difficulty satisfying their infants' hunger. In a later study (Maekawa, Nara, Soeda, Yokoi, & Kitani, 1984Go), in which 6-day-olds were videotaped, first after being breast-fed and again after being bottle fed, findings revealed that subsequent to breast-feeding, infants showed greater ease falling asleep and maintained deeper sleep. Whether breast-fed one-week-olds also show superior behavior while in wakened states of arousal is unknown and the central question of the present investigation. Toward a secondary goal, we examined whether infants of adolescent mothers were differentially affected by feeding method. When controlling for birth weight and perinatal risk factors, comparisons between infants of adolescent and of adult mothers have revealed no differences (Lester, Garcia-Coll, & Sepkoski, 1983Go; Sandler, Vietz, & O'Connor, 1981Go). Since those studies did not report or control for feeding method, it is unknown whether differences would emerge if feeding method were taken into account.

Finally, following earlier work documenting greater irritability and poorer neurobehavioral functioning in breast-fed than formula-fed neonates (DiPietro, Larson, & Porges, 1987Go), the present investigation addressed whether this pattern would be evident at one week, when outcomes are less likely to be artifacts of hunger. In line with evidence suggesting breast-feeding's benefits to infants' immune functioning, physiological development, and sleep behavior, we hypothesized that breast-fed infants would demonstrate superior performance on the BNBAS. By including a sample of infants of adolescent mothers, we sought to add to the few available data about this group of infants, although prior comparisons across maternal age did not lead us to expect differences.


    Method
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 Abstract
 Introduction
 Method
 Results
 Discussion
 References
 
Participants
Following approval from the institutional review board of a "baby friendly" hospital, where unrestricted breast-feeding is heavily advocated, mother/infant dyads were recruited on the maternity unit and administered consent to take part in research on neonatal behavior. Exclusion criteria included drug or alcohol abuse, logistics that would interfere with data collection (such as living outside of the city limits), birth complications, prematurity, cesarean delivery, and any condition (either physical or psychological) requiring medication, since this may have resulted in biased influences on breast-fed infants. Priority was given to adolescent mothers, especially those who were breast-feeding, given their relative scarcity (Wambach & Cole, 2000Go). Of women invited to participate, 14.33% refused. Of these, 92.22% indicated that they were too close to being discharged, and 6.1% indicated that they were too sleepy or in too much pain. Women who refused did not differ from those who agreed on age, parity, feeding method, or infant sex.

Within a week of discharge, mothers who were adolescent (15–18 years) and adult (20–28 years) were identified. Mothers over 28 years were excluded in order to yield contrasts based on more comparable groupings. The appointment clerk also screened out mothers who were no longer breast-feeding exclusively, and then obtained assurances from all mothers that their infants were doing well, brief demographic data, and agreement to refrain from feeding their infants during the visit. As expected (Wambach & Cole, 2000Go), a greater proportion of adolescents than adults were excluded for having terminated breast-feeding or for partially breast-feeding. Demographic characteristics of the breast- and formula-feeding dyads are presented in Table I. Preliminary analyses revealed, as expected (Dennis, 2002Go), that formula-feeding mothers were of lower SES.


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Table I. Demographics of Breast- and Formula-Feeding Groups, Means (SD)
 

Procedure
Home visits were scheduled 7 to 11 days after delivery, 1 to 2 hours after an infant's last feeding, in late morning or early afternoon time slots. After verifying that the infant was in good health and securing a quiet location, usually the master bedroom, the examiner (S.C. or Y.M.) administered the BNBAS on infants in each of the four groupings. The examiners were unaware of the study's goals and had been trained on the BNBAS by the first author, who had been trained at an infant laboratory (Hart, Field, & Nearing, 1998Go). Interrater reliability between the three researchers had been achieved at 93% (where agreements were calculated as item scores ±1 point/total score) prior to the study. Thereafter, this level of interrater reliability was checked on 28 infants, including 7 from each of the four groups, representing 33.74% of the entire sample.

Measures
Demographic Information. These questionnaires addressed maternal age, parity, ethnicity, and education. Scores for SES were derived on the basis of participants' income and education, yielding values ranging from 1 to 6, with higher scores signifying lower socioeconomic status (Hollingshead, 1975Go).

Obstetric Complications Scale (OCS) and Postnatal Scale (PNS). The 41-item OCS and the 10-item PNS (Littman & Parmelee, 1978Go) quantify obstetric and perinatal complications. Items are rated on the basis of medical chart review. The charts were also accessed separately for information such as birth weight, gestational age, and Apgar scores.

Brazelton Neonatal Behavioral Assessment Scale. Neurobehavioral functioning of the newborn is evaluated by an examiner. The 28 items of the BNBAS (Brazelton & Nugent, 1995Go) are scored on 9-point scales and then subjected to clustering techniques which yield summary scores for habituation, orientation, motor, range of state, regulation of state, and autonomic stability. Additional summary scores index atypical responses, including abnormal reflexes, depression, and withdrawal (Lester, Als, & Brazelton, 1982Go; Lester, Freier, & LaGasse, 1995Go).


    Results
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 Abstract
 Introduction
 Method
 Results
 Discussion
 References
 
Following the prediction that breast-feeding would be advantageous to infant behavior, independent of maternal age, a MANCOVA (multivariate analysis of covariance), with feeding method (breast/bottle) and age group (teen/adult) as independent variables and SES as a covariate, was conducted on the nine BNBAS cluster scores. Significant effects for feeding method, F(9, 70) = 5.53, p < .001, permitted further univariate analyses. These revealed breast-fed infants' superiority on seven of the nine clusters, including orientation, F(1, 78) = 8.13, p < .01; motor, F(1, 78) = 4.09, p < .05; range of state, F(1, 78) = 4.65, p < .05; regulation of state, F(1, 78) = 6.70, p < .01; abnormal reflexes, F(1, 78) = 4.87, p < .05; depression, F(1, 78) = 18.91, p < .001; and withdrawal, F(1, 78) = 24.81, p < .001.

To identify individual items which drove these effects, ANCOVAs (analyses of covariance) using feeding method as the independent variable and SES as the covariate were conducted on each of the items separately. These analyses revealed that breast-fed infants' higher scores on the orientation cluster stemmed from their greater abilities to attend to both visual and auditory stimuli, as well as superior qualities of overall alertness. Their higher motor scores reflected their more optimal capacities for smooth and unrestricted movement, more robust ability to defend against interference with breathing, and more appropriate levels of activity. Superiority on the range of state cluster was driven by findings that following high degrees of upset, breast-fed neonates were more able to return to moderate states of arousal. They were also more able to face aversive stimuli with greater degrees of control, show more appropriate amounts of change in levels of arousal, and use hand-to-mouth movements as a self-comforting measure. By contrast, formula-fed neonates demonstrated more abnormal reflexes, suggesting under-reactive responses. They also demonstrated more withdrawal symptoms, such as hyperactive rooting and excessive high-pitched crying. Overall, these results depict breast-fed infants as more alert, responsive, and calm, while formula-fed infants appeared less responsive and fussier. Table II presents data on analyses which were significant.


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Table II. Brazelton Neonatal Behavioral Assessment Scale Scores for Items which Differed Significantly between Feeding Groups
 


    Discussion
 Top
 Abstract
 Introduction
 Method
 Results
 Discussion
 References
 
Contrary to earlier comparisons on the BNBAS between breast- and formula-fed newborns (DiPietro, Larson, & Porges, 1987Go), the present investigation uncovered no evidence of greater irritability in breast-fed one-week-olds. Rather, these infants consistently surpassed formula-fed newborns, and the differences were dramatic. As predicted, these results support findings on sleep behavior in infants of similar ages (Maekawa et al., 1984Go), and are in line with evidence of breast-feeding's advantages to physiological and immunological functioning. Further, the pronounced group differences on the activity, depression, and withdrawal items, which again favored breast-fed infants, corroborate DiPietro and associates' (1987Go) suggestion that formula may have a depressant effect on newborn behavior. Finally, as expected, our findings revealed no evidence that effects of feeding method differ with maternal age.

Breast-fed infants' superior performance could have been related to their mothers' higher SES, though our taking this factor into account statistically detracts from this interpretation. Based on findings that women who choose to breast-feed also engage in greater health-enhancing behaviors in general, it is possible that the breast-fed infants' better behavior is attributable to exposure to superior prenatal conditions (Pesa & Shelton, 1999Go). Since breast-feeding entails more physical contact compared with formula feeding, which entails greater auditory stimulation (Lavelli & Poli, 1998Go), some of the results could have also stemmed from differences in very early interaction experiences which are inherently associated with the two feeding methods and are possibly even linked with culture or ethnicity. Other possible influences pertain to feeding behaviors, such as sucking, feeding frequency and duration, and caloric intake. It is also possible that variation in breast milk biochemistry was a factor, as suggested by research showing that vitamin B6 in human milk is linked to optimized infant behavior, while the presence of alcohol was associated with compromised outcomes (Boylan, Hart, Porter, & Driskell, 2002Go; Schuetze, Das Eiden, & Chan, 2002Go). In addition to calling for investigative attention to underlying mechanisms such as these, the results underscore the need for researchers to be cognizant of feeding-method effects, as these may confound results in other kinds of investigations. For example, some aspects of compromised neonatal functioning which have been attributed to exposure to postpartum depressed mothers (Lundy et al., 1999Go) appear to overlap with those stemming from exposure to formula. Finally, and most importantly, these findings are relevant to clinicians working with women during pregnancy. In addition to promoting breast-feeding on the basis of its known benefits to infant health, it can be advanced on the basis of findings that breast-fed infants are more alert and responsive, and thus more likely to facilitate favorable parental attention and the formation of attachment (Brazelton & Nugent, 1995Go; Hart, Field, & Nearing, 1998Go). Conversely, bottle feeding can be discouraged on the basis of findings that exposure to formula is linked with more sluggish and difficult infant behavior, which may be less rewarding to parents and less conducive to attachment formation.


    Acknowledgments
 
Support received through a Texas Tech University Special Seed Grant for Multidisciplinary Research is greatly appreciated.

Received December 12, 2002; revision received February 27, 2003; accepted April 21, 2003


    References
 Top
 Abstract
 Introduction
 Method
 Results
 Discussion
 References
 
Bernal, J. (1972). Crying during the first 10 days of life, and maternal responses. Developmental Medicine and Child Neurology, 14, 362 –372.[ISI][Medline]

Boylan, L. M., Hart, S., Porter, K. B., & Driskell, J. A. (2002). Vitamin B-6 content of breast milk and neonatal behavioral functioning. Journal of the American Dietetic Association, 102, 1433 –1438.[CrossRef][ISI][Medline]

Brazelton, T. B., & Nugent, J. K. (1995). Neonatal behavioral assessment scale. Cambridge: Mac Keith.

Dennis, C. L. (2002). Breastfeeding initiation and duration: A 1990–2000 literature review. Journal of Obstetric, Gynecologic, and Neonatal Nursing, 31, 12 –32.[CrossRef][ISI][Medline]

DiPietro, J., Larson, S., & Porges, S. (1987). Behavioral and heart rate pattern differences between breast-fed and bottle-fed neonates. Developmental Psychology, 23, 467 –474.[CrossRef]

Dollberg, S., Lahav, S., & Mimouni, F. (2001). A comparison of intakes of breast-fed and bottle-fed infants during the first two days of life. Journal of the American College of Nutrition, 20, 209 –211.[Abstract/Free Full Text]

Hart, S., Field, T., & Nearing, G. (1998). Depressed mothers' neonates improve following the MABI and a Brazelton demonstration. Journal of Pediatric Psychology, 23, 351 –356.[Abstract/Free Full Text]

Hollingshead, A. (1975). Four factor index of social status. Unpublished manuscript. New Haven: Yale University Department of Sociology.

Lavelli, M., & Poli, M. (1998). Early mother-infant interaction during breast- and bottle-feeding. Infant Behavior and Development, 21, 667 –684.[CrossRef]

Lester, B. M., Als, H., & Brazelton, T. B. (1982). Regional obstetric anesthesia and newborn behavior: A reanalysis toward synergistic effects. Child Development, 53, 687 –692.[CrossRef][ISI][Medline]

Lester, B., Garcia-Coll, C., & Sepkoski, C. (1983). A cross-cultural study of teenage pregnancy and neonatal behavior. In T. Field & A. Sostek (Eds.), Infants born at risk: Physiological, perceptual, and cognitive processes (pp. 147 –169). New York: Grune & Stratton.

Lester, B., Freier, K., & LaGasse, L. (1995). Prenatal cocaine exposure and child outcome: What do we really know? In M. Lewis & M. Bendersky (Eds.), Mothers, babies, and cocaine: The role of toxins in development (pp. 19 –39). Hillsdale, NJ: Erlbaum.

Littman, B., & Parmelee, A. (1978). Medical correlates of infant development. Pediatrics, 61, 470 –474.[Abstract]

Lundy, B., Jones, N., Field, T., Nearing, G., Davalos, M., Pietro, P., et al. (1999). Prenatal depression effects on neonates. Infant Behavior and Development, 22, 119 –129.

Maekawa, K., Nara, T., Soeda, A., Yokoi, S., & Kitani, N. (1984). Breastfeeding and neonatal behavioral state. Jikeikai Medical Journal, 31, 503 –509.[Medline]

Pesa, J. A., & Shelton, M. M. (1999). Health-enhancing behaviors correlated with breastfeeding among a national sample of mothers. Public Health Nursing, 16, 120 –124.[CrossRef][ISI][Medline]

Sandler, H., Vietz, P., & O'Connor, S. (1981). Obstetric and neonatal outcomes following intervention with pregnant teenagers. In K. Scott, T. Field, & E. Robertson (Eds.), Teenage mothers and their off-spring (pp. 16 –32). New York: Grune & Stratton.

Schuetze, P., Das Eiden, R., & Chan, A. W. K. (2002). The effects of alcohol in breast milk on infant behavioral state and mother-infant feeding interactions. Infancy, 3, 349 –363.[CrossRef]

Wambach, K. A., & Cole, C. (2000). Breastfeeding and adolescents. Journal of Obstetric, Gynecologic, and Neonatal Nursing, 29, 282 –294.[CrossRef][Medline]


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