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TABLE 4. Studies of the secondary preventive effects of breastfeeding
|Study||Study design||Sample||Exclusion criteria||Outcome variables||Significant results|
|Lucas et al., 1989 ||Prospective, longitudinal, randomized trial compar- ing the effects of donated BBM and PTF on the be- havioural development of pre-tenm infants. Subjects received the treatment until discharge from the hospital or until attaining a weight of 2,000 g Data on behaviour obtained at 9 mo Subjects classified into 2 groups according to mother's decision to breastfeed or not to breastfeed Within each group, subjects randomly assigned to receive BBM or PTF via nasogastric tube while in hospital Treatment was given as a supplement to mother's milk to infants whose mothers chose to breast feed, and as sole diet to in- fants whose mothers chose not to breastfeed||502 pre-term infants born in 3 hospitals in England and admitted to special care unit No. of subjects included in final analysis: Breastfed group: mother's milk + BBM (n = 170); mother's milk + PTF (n = 173) Not breastfed group: BBM only (n = 83); PTF only (n = 76)||Birthweight >1,850 g Major congenital anomalies||Scores on developmental screening inventory of Knobloch et al. at 9 mot Five areas of behaviour assessed: adaptive be- haviour, gross motor fine motor, language and personal-social Overall DQ obtained by averaging scores on all scales||Comparisons for all subjects receiv ing BBM vs subjects receiving PTF at 9 mo regardless of whether or not they received mother's milk:|
|*p < .05; **p < .025|
|Comparisons for subjects receiving treatment as supplement to mother's milk (breasfed group):|
|*p < .05; **p < .025|
|Comparisons for subjects receiving treatments as sole diets (not breasfed group) were not significant|
|Lucas et al., 1994 ||Prospective, longitudinal, randomized trial compar- ing the effects of donated BBM and PTF on the cog- nitive and motor develop- ment of pre-tenm infants Data on cognitive and motor performance gathered at 10 mo Subjects classified mto 2 groups according to mother's decision to breastfeed or not to breastfeed Within each group, subjects randomly assigned to receive BBM or PTF via nasogastric tube while in hospital Treatment was given as a supplement to mother's milk to infants whose mothers chose to breast feed, and as sole diet to infants whose mothers chose not to breastfeed||502 pre-term infants born in 3 hospitals in England and admitted to special care unit No. of subjects included in final analysis: Breastfed group: mother's milk + BBM (n = 134); mother's milk + PTF (n = 139) Not breastfed group: BBM only (n = 62); PTF only (n = 52)||Birthweight >1,850 g Major congenital anomalies||Bayley MDI and PDI scores at 18 mo||No significant effects of treatment type (BBM or PTF) or of pres ence or absence of breastfeeding on MDI or PDI scores|
|Lucas et al., 1992 ||8-yr follow-up of cognitive development of pre-term infants participating in 2 prospective randomized clinical triais Trial 1 compared the effects of regular formula and PTF on cognitive and motor performance of pre-tenm infants at 10 mo Tnal 2 compared the effects of BBM and PTF on cog- nitive and motor perfor mance of pre-tenm infants at 9 and 18 mo||300 children 7.5-8 yr old bonn pre-tenm and admitted to special care unit at 5 hospitals in England||Birthweight >1,850 g Major congenital anomalies||Scores on abbreviated WISC-R Test at 7.5-8 yr .||Mean score advantages for breasfed vs not breastfed children on various WISC-R scales:|
|p < .001|
|Analyses for randomization trial outcomes (e g., regular formula reported|
|Lucas et al., 1992 ||Treatment was given as a supplement to mother's milk to infants whose mothers chose to breast feed, and as sole diet to in fants whose mothers chose not to breastfeed Subjects classified in 2 groups according to whether or not they were breastfed: breastfed + treatment (n = 210); not breastfed (treatment only) (n = 90) Data on cognitive perfor mance obtained at 7.5-8 yr|
|Lanting et al., 1994 ||Retrospective correlational study examining the rela- tion between infant-feed- ing method and develop- ment of neurologic disorders in childhood Subjects classified soon after birth as having normal, slightly abnormal, or frankly abnormal neuro- logic status on the basis of a standardized neurologic examination Subjects selected for follow up given a standardized neurologic examination at 9 yr Subjects classified according to infant-feeding practices on the basis of a question naire completed by parents: formula-fed (n = 358); breastfed with formula supplement at least 3 wk (n = 33); exclusively breastfed at least 3 wk (n = 135)||Selected from cohort of 3,162 infants bonn 1975-78 in a hospital in the Netherlands||Feeding data in- complete Mother could not recall feeding practices Pre-term infants Infant admitted to special care ward||Performance on neuro- logic examination at 9 yr Neurologic status classi- fied as: normal, minor dysfunction-grade I (fewer symptoms), minor dysfunction- grade 2 (more symp- toms), or abnormal||For analysis, subjects breastfed with formula supplement at least 3 wk were combined with subjects exclusively breastfed at least 3 wk For all subjects breastfed at least 3 wk, regardless of neurologic classification at birth, scores on the 9-yr neurologic examination and the likelihood of being classified as normal at 9 yr were higher|
|Menkes, 1977 ||Retrospective, cross-sec- tional, correlational study examining the relation between infant-feeding method and development of learning disabilities in childhood Subjects were classified as those with learning dis- orders and a control group of children with other neurologic disorders Breastfed children defined as those receiving breastmilk for at least 4 wk||Learning disorder sub- jects were 29 white, middle-class chil- dren born 1959-70 and referred to author for neuro- logic assessment and treatment Control subjects were patients of the author who pre sensed with a variety of other neurologic disorders Subjects matched by sex and age (n = 53)||Pre-term infants (no definition provided) Major congenital malformations Infants whose feeding methods were determined by circumstances||Subjects in the learning disorder and control groups were classified as breastfed or boale- fed||13.8% of children with learning disorders and 47.2% of control children were breastfed (P = .004)|
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 . 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.  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.  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  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.  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  (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 . 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 . Of importance here is that marijuana appears in the milk of lactating women who use the drug . 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.
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
|Study||Study design||Sample||Exclusion criteria||Outcome variables||Significant results|
|Little et al. 1989 ||Prospective, longitudinal, correlational study examin- ing the effects of maternal alcohol use during lactation on infant mental and motor development Cognitive and motor develop- ment measured at 12 mo Maternal alcohol use measured by questionnaire during mo 1 and 3 Breastfed children defined as those receiving the majority of intake from breastmilk (<16 oz/day of non-human milk or supplement)||400 infants, mostly white and middle-class, born to mothers belonging to a health maintenance organization in Seattle, Washington, USA||No prenatal care before 6 mo gestation||Bayley MDI and PDI scores at 12 mo Independent variable: Infant AA score, used to indicate infant's ex- posure to alcohol via breastmilk, estimated from mother's reports of daily alcohol con- gumption and days of breastfeeding per month during mo 1 and 3||Infant AA score not related to MDI scores at 12 mo Significant linear trend found for effects of infant AA score on PDI score at 12 mo (p < .006)|
|Astley and Little, 1990 ||Longitudinal, correlational study examining the relation between maternal marijuana use during lactation and cognitive and motor devel- opment of infants Cognitive and motor perfor- mance measured at 12 mo breastfed children defined as those receiving the majonty of intake from breastmilk (<16 oz/day of non-human milk or supplement) for at least 2 wk||323 infants, mostly white and middle-class, born to mothers belonging to a health maintenance organization in Seattle, Washington, USA||Infants not breastfed at least 2 wk Infants who did not have 12-mo assessments||Bayley MDI and PDI scores at 12 mo Independent variable: Infant's exposure to matemal marijuana use during lactation esti- mated from mother's reports of daily mari- juana use and days of breastfeedmg per month during mo 1 and 3 .||No significant effect of exposure to marijuana on MDI scores at 12 mo Mean PDI scores at 12 mo according to days of exposure to maternal marijuana use during Ist month postpartum:|
|Mean difference between groups with 0 and 1-14 days exposure and group with 15-30 days exposure is significant (p < .005).|
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.  and the controlled study by Agostoni et al.  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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