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TABLE 4. Studies of the secondary preventive effects of breastfeeding

A natural conclusion from this study is that at nine months of age, pre-term babies who were fed a PTF with the specifications listed had a developmental advantage over those fed BBM. The authors note that part of the developmental importance of this finding is that the screening inventory includes many of the items of the Gesell Schedule, which is a good predictor of later intelligence. However, in contrast to this claim, a vast body of literature on infant development shows that the predictive validity of developmental scales administered during the first 12 months of life is not different from zero [11]. In our view, the reported differences in the performance of preterm infants fed PTF and BBM are anecdotally interesting but of limited developmental significance over the long term.

In a follow-up at 18 months of age, Lucas et al. [35] assessed 387 of the infants in the original sample with the Bayley MDI and PDI scales. In contrast to the nine-month follow-up, no advantage was found for subjects receiving PTF; infants fed with BBM performed about as well as subjects receiving PTF on both the MDI and PDI scales. Additionally, no significant differences were found for MDI or PDI scores when the subjects were grouped according to whether or not they received mother's milk as a supplement. The authors suggest that the failure to find results in the same direction as the nine-month follow-up may be due to the subjects' recovery from earlier nutritional deficiencies.

In a 1992 article, Lucas et al. [36] reported the effects of breastmilk fed to pre-term babies on intelligence quotients obtained seven to eight years later (table 4). In this second study, the subjects were admitted to the special-care baby units in Cambridge, Ipswich, Kings Lynn, Norwich, and Sheffield between January 1982 and March 1985. Two of these care units (Norwich and Sheffield) were not included in the study published in 1989. Also, in the first study the subjects were selected up to 1984, whereas in this second study the recruitment extended to March 1985. The authors do not specify the degree of overlap between the subjects in the 1994 study [35] and those in the present study. However, they do suggest that both fall out from the same clinical trial and follow the same design. One feature of the 1992 publication is that it does not include data on the subjects who received only BBM.

At 7 1/2 to 8 years of age, the subjects who had received milk expressed from their own mothers (group 2) had higher IQs than the children whose mothers chose not to provide breastmilk for them (group 1). In particular, the differences were observed in the Verbal Performance and Overall Scale (group 1, 92.8; group 2, 103) of the Wechsler Intelligence Scale for Children. According to an analysis within group 2 of the subjects who received breastmilk from their mothers in comparison with those who did not, the overall IQ of this last subgroup (94.8) was similar to that of group 1 (92.8), and both groups had significantly lower IQs than children whose mothers were successful in expressing milk (103.7). A final analysis restricted to the children of the successful mothers showed a dose-response relationship between mother's milk and subsequent IQ.

In conclusion, feeding maternal milk to pre-term babies with very low birthweights improved their middle-childhood IQs, as compared with IQs of preterm babies who did not receive maternal milk (and who received PTF, mature, pasteurized donor drip breastmilk, or term formula). The authors concluded that the data supported the causal hypothesis that breastmilk promotes the neural development of pre-term babies. They found additional support for their hypothesis in the existing information that human milk contains various factors, such as long chain lipids, that might affect nervous system development. This impressive set of findings requires confirmation by other laboratories and a control for the extent to which the mothers who succeeded in expressing milk did or did not differ in their childrearing practices from the remaining mothers.

Lanting et al. [38] studied the relation between feeding method and necrologic functioning at nine years of age (table 4). Three groups of children were formed on the basis of a neonatal neurologic examination. One group (n = 160) was defined as neurologically abnormal (e.g., hemisyndrome, hypotonia, hypertonia) at birth; a second group consisted of a random sample of children (n = 322) with minor abnormalities (e.g., mild hypotonia); and a random sample of normal children formed a third group (n = 322). Nine years after birth, a standard neurologic examination was given to the children in the three groups and they were again reclassified as normal, having minor neurologic dysfunction (two categories), or abnormal. In addition, information was obtained at this new examination on early feeding practices, and three feeding groups were formed: exclusively formula-fed, breastfed plus formula-fed within the first three weeks of birth, or exclusively breastfed for at least three weeks.

Across groups, at nine years of age the children who had been exclusively breastfed were neurologically better off than the formula-fed children. Moreover, among the children classified with minor neurologic dysfunction during the neonatal period, those who had been breastfed were less likely to have minor neurologic dysfunction. In particular, the frequency of minor neurologic abnormalities was twice as high for formula-fed children as for those who were breastfed. The authors suggested that the type of feeding during the first weeks of life plays a role in later neurobehavioural development.

Of interest here is a retrospective study published in 1977 which showed that early feeding history predicted learning disorders [39] (table 4). The frequency of breastfeeding was compared in two groups of children: 29 children referred to a paediatric neurologist because of learning disorders and 53 children seen in the same office because of neurologic conditions other than learning disorders. In the latter group, 47.2% of the children had been breastfed, compared with only 13.8% in the former group. The intent of this comparative study was to test the hypothesis that the high protein content (1.5 to 3.3 g/100 ml) of the formula contributed to the evolution of learning disorders.

Breastmilk as risk factor (table 5)

Two studies are reviewed here that address the question of whether breastmilk operates as a risk factor by the transfer of toxic substances from the mother to the infant [40, 41]. Because of their correlational nature, these studies have limitations in design similar to those discussed above regarding the direct effects of breastmilk. There is no way of discriminating between group differences due to the independent variable and those due to confounders, nor can the effects associated with the prenatal and postnatal periods be separated. A particular concern is whether the use of a toxic substance is associated with caretaking behaviours that hinder rather than foster development.

The first study was a prospective, longitudinal study that tested the effects of alcohol consumption during the lactation period on mental and motor development at 12 months of age [40]. The subjects were 400 middle-class infants. The independent variable was represented by a score that indicated the infant's exposure to alcohol through breastmilk. Maternal reports of daily alcohol consumption were obtained along with reports of the number of breastfeeding days per month. These scores were then related to the Bayley PDI and MDI scores at 12 months of age. A statistically significant linear trend was observed between alcohol consumption and PDI. A comparison of the end points of this continuum shows a difference of 19 PDI points (>1 standard deviation) between infants of mothers who consumed no alcohol and those with the highest consumption.

The second study, which was also longitudinal and correlational, examined the potential effects of the use of marijuana during lactation on the mental and motor development of the offspring [41]. Of importance here is that marijuana appears in the milk of lactating women who use the drug [42]. The criterion for inclusion in the study was breastfeeding for at least two weeks. As in other studies, the Bayley MDI and PDI scores were obtained from all infants at 12 months of age. Again, although there were no differences between children of users and non-users of marijuana in the MDI, there was a clear trend in the expected direction for the PDI. The mean PDI of the infants of mothers with 0 days of exposure was 102, whereas that of the infants with 15 to 30 days of exposure was 90.

As noted, inherent limitations of correlational studies prevent conclusive inferences. Moreover, even under controlled conditions, data from two studies alone are generally insufficient to guide policy. Therefore, definitive recommendations regarding breastfeeding for mothers who consume alcohol and marijuana are unwarranted. However, the findings are suggestive and indicate a need for further information.

General discussion

Breastfed children have a modest advantage over artificially fed children in developmental scales, IQ tests, and tests of particular cognitive processes. Although no definitive conclusions on causality are warranted, the consistency of the findings across studies carried out in different populations and social contexts is quite remarkable. These suggestive findings point to the need for experimental studies leading to conclusive statements.

In addition to limitations of design, the studies have had a restricted focal concern, first, on main effects, and second, on products of development such as IQ or psychomotor indexes. Possible differential effects of breastfeeding as a function of contextual (e.g., social and economic) factors and organismic status have been disregarded. There is also suggestive evidence that the duration of breastfeeding may have an effect.

Rather than focusing on developmental outcomes, studies should also examine the contributions of breastfeeding to the processes of development. In this line of reasoning, we believe that a particular area of enormous potential is the assessment of the role of breastfeeding in the formation of secure attachment in early childhood. Besides their universality, breastfeeding and attachment have had significant evolutionary value, and their interconnectedness could well have served human adaptation.

TABLE 5. Studies of breastmilk as a risk factor

The suggestive evidence that breastmilk contributes to the healthy mental development of premature infants is impressive. Moreover, the use of breastmilk as an experimental variable provides guidelines for future research with at-risk and normal newborns. Even though the data refer to premature infants with very low birthweight, these findings contradict much of the contemporary theorizing and research data on the causes and risk factors of development. As noted above, we accept that the causes of development are multiple and interactive, and that individuals reach the same end point by different developmental trajectories [43, 44]. It is indeed curious that differences in feeding for 27 days could orient development along very different courses. There is a great need to replicate these findings, which are of major importance to clinical paediatrics.

The external validity of these data is limited, and their relevance for populations where malnutrition is endemic is questionable. The high prevalence of low birthweight in third world countries is attributed primarily to the number of small-for-date newborns [45, 46]. Pre-term birth is a condition that is more prevalent in industrialized societies. The pathophysiology of prematurity is different from that of intrauterine growth retardation.

A natural extension of the data on pre-term babies is the idea that breastmilk operates as a secondary preventive factor. Pre-term babies will benefit from breastmilk because it is rich in LC-PUFA, particularly docosahexaenoic acid, an essential component in the development of the visual system and cerebrum. The correlational work by Lanting et al. [38] and the controlled study by Agostoni et al. [32] support this notion.

The nutritional and immunologic value of human milk is well established, and the suggestive evidence of beneficial behavioural consequences fits with our understanding of the physiological processes involved in lactation. Societal changes, economic pressures, and technological advancements, however, could impose limitations in some instances on the value of human milk. It is plausible that breastmilk transfers drugs and chemicals used by the mother to the nursing infant, which could have adverse developmental consequences. The data on alcohol and marijuana which we reviewed are insufficient to draw any conclusive inferences, but they certainly post a sign for caution.

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