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Department of Neurology,
* Perinatal Nutrition and Development Unit, Department of Obstetrics and Gynaecology and
** Department of Pathology and Laboratory Medicine, University Hospital, University of Groningen, Groningen, The Netherlands and
Numico Research Germany, Friedrichsdorf, Germany
2 To whom correspondence should be addressed. E-mail: m.hadders-algra{at}med.rug.nl.
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ABSTRACT |
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 TOP ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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6 wk. In the group of infants breastfed for 
6 wk (n = 55), 18% exhibited normal-optimal GM, 47% normal-suboptimal GM, and 47% mildly abnormal GM. In contrast, in the group of infants breastfed for > 6 wk (n = 92), 43% exhibited normal-optimal GM, 45% normal-suboptimal GM, and 12% mildly abnormal GM. Exclusive breastfeeding for >6 wk was therefore associated with markedly less abnormal and more normal-optimal GM. Thus, we conclude that breastfeeding for > 6 wk might improve the neurological condition in infants.
KEY WORDS: • breastfeeding • general movements • development • term infant
In general, breastfed infants show better cognitive development than formula-fed infants (1). In addition, cognitive function improves with the duration of breastfeeding (1). Whether the same holds true for neurological condition is uncertain. Lanting et al. (2) retrospectively collected information on the duration of breastfeeding in a mixed population of infants with and without risk for developmental disorders that were followed from birth. They reported that breastfeeding for 
3 wk was associated with better neurological condition at 9 y than formula feeding (2). In a prospective study, Lanting et al. (3) indicated that children exclusively breastfed for 6 wk moved more fluently at 3.5 y than did formula-fed age-matched controls. However, the Lanting studies did not address the question of the minimum duration of exclusive breastfeeding needed to achieve optimal neurological condition. The present paper addresses this question.
We recently conducted a double-blind randomized trial on the effect of feeding formula supplemented with long-chain PUFA (LC-PUFA)2 on the quality of general movements (GM) in healthy term infants (4). The quality of GM is a recently developed sensitive instrument for the assessment of brain function in young infants (5,6). General movements are spontaneous movements of the young infant involving all parts of the body. Normal GM are characterized by variation, complexity and fluency. These characteristics disappear when movements become abnormal. Movement fluency is the first property to disappear, indicating that subtle dysfunctions of the nervous system already cause jerky or stiff movement at this early phase of development. Movement complexity and movement variation, which in fact can be considered as two forms of variation, are the major characteristics of GM quality. Four classes of GM-quality can be distinguished: two forms of normal GM (normal-optimal and normal-suboptimal) and two forms of abnormal GM (mildly and definitely abnormal). The quality of GM at the age of 3 mo is a powerful predictor of neurological outcome. Definitely abnormal GM at 3 mo predicts the development of cerebral palsy with an accuracy of 85 to 98%, whereas the presence of mildly abnormal GM at 3 mo is associated with increased risk of minor neurological dysfunction and attention problems at school age (5–7).
Bouwstra et al. (4) studied three groups of newborn infants (n = 397) for the first 2 mo; 119 infants were fed formula supplemented with LC-PUFA, 131 infants were fed control formula and 147 infants were breastfed. Infants fed control formula markedly more often exhibited mildly abnormal GM than did the infants of the other two groups (31% vs. 19 to 20%). Thus, LC-PUFA supplementation had a beneficial effect on the quality of GM. The breastfed infants (the reference group) more often exhibited normal-optimal GM (34% vs. 18 to 21%). The present report examines the breastfed reference group only and aims to determine the minimum duration of breastfeeding needed to achieve optimal GM quality.
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MATERIALS AND METHODS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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= 0.75; (10)]. Statistical methods.
Statistical analyses focused on the effect of duration of exclusive breastfeeding on the presence of mildly abnormal GM and normal-optimal GM. In addition to univariate statistical analysis with 
2 or Fisher’s exact test, two runs of binary logistical regression analysis were carried out to adjust for potential confounders, one analyzing the effect of the duration of exclusive breastfeeding on the presence of normal-optimal GM and the other analyzing the effect of the duration of breastfeeding on the occurrence of mildly abnormal GM. Variables describing the social condition (see Table 1) and the variables of the OOS were also included in the multivariate analysis. In the univariate analyses of the relationship between duration of exclusive breastfeeding and quality of GM, P-values of <0.0167 (Bonferroni correction: 0.05/3; two tailed) were considered significant; in the other analyses P-values of 0.025 (two tailed) were considered significant.
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RESULTS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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6 wk. Quality of GM was significantly better in infants breastfed for 6 wk than in those breastfed for 6 wk (Table 2; Fig. 1). The social, but not the obstetrical, background of mothers who breastfed for > 6 wk differed from that of mothers who breastfed for a shorter period. As expected, longer breastfeeding was associated with a higher level of parental education and professional employment, less paternal smoking and greater maternal alcohol consumption (Table 1). Logistical regression analyses confirmed that breast-feeding for >6 wk was associated with the presence of less mildly abnormal GM (P < 0.0015; explained variance 6.9%) and more normal-optimal GM (P < 0.0025; explained variance 6.8%). None of the potential confounders, including duration of LC-PUFA supplementation, contributed significantly to the models.
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DISCUSSION |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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6 wk is associated with a beneficial effect on the quality of GM at the age of 3 mo. This finding is of clinical relevance because the quality of GM correlates with neurobehavioral condition at school age (5,6). It is important to realize that we report an association, which does not necessarily imply causation. However, a study to demonstrate causation cannot be performed, because randomized trials on breastfeeding are not ethically justified. Three explanations can be offered for the association between longer duration of breastfeeding and better neurological condition. First, it may be that infants with better neurological condition are more likely to be breastfed for a longer duration. Second, the association could be mediated by a difference in nurturing habits between the two groups, as nurturing habits (e.g., bonding) can affect neurobehavioral development. However, it is interesting to note that Lucas and Morley (11) found that the intelligence quotient of children who had been fed human milk by nasogastric tube was 8 points higher at 8 y than that of children fed formula by nasogastric tube. Third, longer exposure to specific components of breast-milk, such as LC-PUFA, may beneficially affect the rapidly developing brain. At the age of 6 wk, an important period of transition in brain function begins (7,12). This is the onset of the period in which the infant becomes a social partner (13). More important, this is the age at which the quality of GM becomes predictive, indicating that basic neurocircuitries become stabilized (5,6). Based on our finding, we hypothesize that the beneficial effect of breastfeeding continues up to the onset of this period of transition in brain function.
In conclusion, our study suggests that continuation of exclusive breastfeeding for at least 6 wk improves infant neurological condition.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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3 Abbreviations used: GM, general movements; LC-PUFA, long-chain PUFA; OOS, Obstetrical Optimality Score.
Manuscript received 25 June 2003. Initial review completed 12 August 2003. Revision accepted 29 September 2003.
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LITERATURE CITED |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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1. Anderson, J. W., Johnstone, B. M. & Remley, D. T. (1999) Breast-feeding and cognitive development: a meta-analysis. Am. J. Clin. Nutr. 70:525-535.
2. Lanting, C. I., Fidler, V., Huisman, M., Touwen, B.C.L. & Boersma, E. R. (1994) Neurological differences between 9-year-old children fed breast-milk or formula-milk as babies. Lancet 344:1319-1322.[Medline]
3. Lanting, C. I., Patandin, S., Weisglas-Kuperus, N., Touwen, B.C.L. & Boersma, E. R. (1998) Breastfeeding and neurological outcome at 42 months. Acta Paediatr. 87:1224-1229.[Medline]
4. Bouwstra, H., Dijck-Brouwer, D. A., Wildeman, A. L., Tjoonk, H. M., Van der Heide, J. C., Boersma, E. R., Muskiet, F.A.J. & Hadders-Algra, M. (2003) Long-chain polyunsaturated fatty acids have a positive effect on the quality of general movements of healthy term infants. Am. J. Clin. Nutr. 78:313-318.
5. Hadders-Algra, M. (2001) Evaluation of motor function in young infants by means of the assessment of general movements: a review. Pediatr. Phys. Ther. 13:27-36.
6. Prechtl, H.F.R. (2001) General movement assessment as a method of developmental neurology: new paradigms and their consequences. Dev. Med. Child Neurol. 43:836-842.[Medline]
7. Hadders-Algra, M. & Groothuis, A.M.C. (1999) Quality of general movements in infancy is related to neurological dysfunction, ADHD, and aggressive behaviour. Dev. Med. Child Neurol. 41:381-391.[Medline]
8. Touwen, B.C.L., Huisjes, H. J., Jurgens-Van der Zee, A. D., Bierman-Van Eendenburg, M.E.C., Smrkovsky, M. & Olinga, A. A. (1980) Obstetrical condition and neonatal neurological morbidity. An analysis with the help of the optimality concept. Early Hum. Dev. 4:207-228.[Medline]
9. Hadders-Algra, M., Mavinkurve-Groothuis, A.M.C., Groen, S. E., Stremmelaar, E. F., Martijn, A. & Butcher, P. R. (2003) Quality of general movements and the development of minor neurological dysfunction at toddler and school age. Clin. Rehabil. (in press).
10. Landis, J. R. & Koch, G. G. (1977) The measurement of observer agreement for categorical data. Biometrics 33:159-174.[Medline]
11. Lucas, A. & Morley, R. (1992) Breast milk and subsequent intelligence quotient in children born preterm. Lancet 339:261-265.[Medline]
12. Prechtl, H.F.R. eds. Continuity of Neural Functions from Prenatal to Postnatal Life 1984 Blackwell Scientific Oxford, U.K. .
13. Van Wulfften Palthe, T. & Hopkins, B. (1984) Development of the infant’s social competence during early face-to-face interaction: a longitudinal study. Prechtl, H.F.R. eds. Continuity of Neural Functions from Prenatal to Postnatal Life 1984:198-219 Blackwell Scientific Oxford, U.K. .
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