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Food and Nutrition Program, Pan American Health Organization, Washington, DC 20037
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INTRODUCTION |
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 TOP INTRODUCTION The biology of EBF...New scientific evidence on...Developing a public health...REFERENCES |
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). Since then, this recommendation has been reviewed in two
WHO publications (Brown et al. 1998
, Lutter 1992
). In addition, new scientific evidence is available for
both normal and low birth-weight infants (Cohen et al. 1994
, Dewey et al. 1999
). Based in part on this
evidence, UNICEF, the American Academy of Pediatrics
(1997)
, as well as most Ministries of Health in Latin America
have changed their recommendation to 6 mo of age or "about 6 mo."
The actual duration of EBF tends to be quite short in most countries,
although it is increasing in some countries (Lutter, in press). It has
been argued that the 4–6 mo recommendation is too vague and that many
women introduce foods at 2–3 mo so that infants will be "eating
well" by the fourth month (Konis-Booher et al. 1990
).
While this may be correct, the implications of the recommended length
of EBF for maternal breastfeeding behavior have not been studied. The
recommended length of EBF has implications for the Code of Marketing of
Breast-milk Substitutes (WHO 1981
) as it defines the
period during which breast-milk substitutes cannot be promoted
(Article 5.1). Thus, a change in the recommendation to 6 mo from 4–6
mo would extend the period when breast-milk substitutes cannot be
promoted by 2
mo.2
Neither the implications for maternal behavior nor the Code is relevant
for the recommended length of EBF, which should be based solely on
scientific evidence.
The objective of this commentary is to briefly review key issues related to i) the uses of energy balance vs. growth to determine the recommended length of EBF; ii) the merits as well as criticisms of the most recent scientific evidence on its recommended length; and iii) the conceptual and practical issues in using this information to make a public health recommendation.
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The biology of EBF as it relates to infant energy intake and growth. |
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TOPINTRODUCTIONThe biology of EBF...New scientific evidence on...Developing a public health...REFERENCES |
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) and is extremely plastic as demonstrated by the
numbers of women who successfully breastfeed twins and triplets
(Saint et al. 1986
). Based on this evidence, it has been
argued that it is futile to base the length of EBF on the point where
the energy provided by breast milk no longer meets the energy
requirements and that infant growth should be used instead
(Brown et al. 1998
). However, the issues involved in
assessing the recommended length of EBF are sufficiently complex that
both infant nutrient requirements and growth should be considered,
recognizing that both contribute toward a better scientific basis for
this recommendation.
Since the 1979 WHO recommendation was developed, there is general
scientific consensus that recommended energy intakes should be based on
total energy expenditure as assessed by doubly labeled water plus the
energy required for growth (Brown et al. 1998
). The new
estimated energy requirements based on total energy expenditure and
total energy deposition (Butte 1996
) for breastfed
infants are very similar to that provided by breast milk during the
first 6 mo of life in affluent populations and very close to that
provided by breast milk in disadvantaged populations (Brown et al. 1998
). When comparable methods for measuring
breast-milk production have been used, that of poorly nourished
women is remarkably similar to that of well-nourished women
(Brown and Dewey 1992
, Prentice et al. 1986
).
Breastfed infants have a different growth pattern compared to
nonbreastfed infants (Butte et al. 1984
,
Whitehead and Paul 1984
). WHO is currently conducting a
multi-country growth study to develop new growth charts based on
growth patterns of breastfed infants to replace those now widely used
that are based on predominantly nonbreastfed infants (Dewey et al. 1995
). It has been argued that this study will permit a
reassessment of the current WHO recommendation on length of EBF;
however, because it is observational, it is not designed to address the
effect of the feeding regime vs. other factors related to the
mother-infant dyad that affect infant growth. Only research trials
that replicate the studies described below in terms of random design
will provide data relevant to the recommendation. Given its public
health importance, such studies are urgently needed.
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New scientific evidence on the recommended length of EBF. |
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TOPINTRODUCTIONThe biology of EBF...New scientific evidence on...Developing a public health...REFERENCES |
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). Since this review was
published, two randomized studies that examined the length of EBF in
infants of normal birthweight (Cohen et al. 1994
) and in
term but low birthweight infants (Dewey et al. 1999
)
have become available. In these studies, infants who were EBF for 4 mo
were randomized into three groups: i) continued EBF on demand; ii)
continued breastfeeding on demand with solid food at 4 mo; and iii)
continued breastfeeding maintaining preintervention breastfeeding
frequency with solid food at 4 mo. All foods were hygienically prepared
and nutritionally adequate. The main outcomes were infant energy intake
and growth in weight and length. The intervention ended when infants
were 6 mo of age.
In normal birthweight infants, the results showed that EBF between 4
and 6 mo resulted in small and statistically nonsignificant increases
in length and weight gain. Between 6 and 12 mo when all infants were
receiving complementary foods, there were no differences in weight or
length gain among the treatment groups. Energy intakes of infants who
were exclusively breastfed for 6 mo were lower but not statistically
different from those in the other two groups. Infants receiving
complementary foods significantly reduced their consumption of breast
milk even in the group that was supposed to maintain breastfeeding
frequency. Infants in all three groups appeared to satisfy their energy
needs as they regularly left breast milk in the breast
(Perez-Escamilla et al. 1995
).
Among low birthweight infants, at 6 mo of age total energy intake did
not differ significantly between the EBF infants and those receiving
complementary foods among the subsample of infants for whom these
measures were available (Dewey et al. 1999
). However,
between 16 and 26 wk the change in total energy intake was
significantly greater in the complementary food groups compared to the
EBF group. With respect to weight and length gain, there were no
significant differences between intervention groups in either the total
sample or subsample for whom dietary intake data are available between
16 and 26 wk; both weight and length gain were slightly greater in the
EBF group. The results did not change when subjects who did not comply
with treatment allocation after randomization were included in the
analysis, which included five subjects in the EBF group and one in the
complementary feeding groups for whom such data were available.
It has been argued that the <10% difference in energy intake among
normal weight infants, though statistically nonsignificant
because of the small sample size, is of theoretical importance and may
be of biological importance with respect to growth (see Table 1 in Frongillo and Habicht 1997
). This argument is not convincing for two reasons: i)
infants in all three groups regularly left breast milk in the breast,
which suggests that their energy needs were met and ii) there were no
statistically differences in growth among the three treatment groups,
and small sample size was not a problem as infants exclusively
breastfed for 6 mo were at a slight advantage with respect to weight
and length, albeit a nonsignificant one.
Another key issue with the study concerns a statistically significant
difference in the number of dropouts between treatment groups in the
normal birthweight study (Frongillo and Habicht 1997
).
Ten from the EBF group vs. 13 for the other two groups combined dropped
out (P = 0.052). In the low birthweight study, there
were eight dropouts in the EBF group and only one in the complementary
feeding group (P = 0.02). Although there was no
indication of insufficient milk intake among normal birthweight infants
who dropped out in the EBF group, one infant was clearly not growing
well between 4 and 5 mo (Frongillo and Habicht 1997
).
The relative importance of this infant compared to the 50 that
completed the study as it affects a public health recommendation is
discussed in the next section. Among the low-birthweight infants,
dropouts were significantly lower in birthweight, head circumference,
Apgar score at 5 min and maternal age (Dewey et al. 1999
). None of these variables was significantly associated
with weight and length gain from 16 to 26 wk except birthweight, which
was negatively correlated with length gain though not weight gain.
Thus, if these infants had been included in the analysis the overall
mean length gain among EBF infants would probably have been greater
than that found among those that finished the study.
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Developing a public health recommendation: conceptual and practical issues. |
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TOPINTRODUCTIONThe biology of EBF...New scientific evidence on...Developing a public health...REFERENCES |
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).
|
). The question of food
acceptability was addressed in the Honduras study, where it was found
that the introduction of complementary foods at 4 vs. 6 mo of age did
not affect food acceptance between 6 and 12 mo of age and that infants
needed very little time to adapt to complementary foods (Cohen et al. 1995
). ii) The recommendation could be made conservatively, based on the age at the lower boundary to ensure that those infants who need complementary foods at the younger ages are covered. Setting the recommendation at 2 SD below the mean age would ensure that the needs of virtually all infants are met. However, it also assumes that there are no risks associated with earlier introduction for those infants who do not need complementary foods until a later time. Such a conservatively based recommendation would meet the needs of the one infant who appeared to be growing poorly between 4 and 5 mo out of 50 infants in the EBF group that completed the study.
iii) Justification could also be made for using the mean age at which nutrient requirements are satisfied by nutrients from EBF on the premise that it represents a public health recommendation based on the mean and, therefore, best reflects the balance between the overall risks and benefits of both too early and too late introduction. As recommended by WHO, any recommendation, including a recommendation regarding the length of EBF, should be tailored to individual infants based on clinical evidence.
Once a consensus is reached on how to describe the length of time EBF can satisfy infant energy and micronutrient requirements and growth, an equally important step is to translate this description into a public health recommendation that is easily understood by health professionals, mothers and their families. Because of the implications of this recommendation for the Code, it also needs a clear legal interpretation. To ensure that the public health recommendation is understood, it is critically important to undertake community-based qualitative research among health professionals, mothers and their families in a number of geographic and economic settings to ensure that it is understood as intended prior to widespread dissemination.
The studies described earlier did not have a group that received
home-prepared complementary foods between 4 and 6 mo. Such foods
are more likely to have been of lower nutritional quality and possibly
contaminated compared to the processed foods provided as part of the
study (Cohen et al. 1994
, Dewey et al. 1999
, Frongillo and Habicht 1997
). Had
such a group been included, it is likely that their growth may have
been compromised with respect to those infants EBF. Frongillo and Habicht (1997)
suggest that in settings where the risks of
infection from nonhygienic complementary foods, a prescriptive
recommendation for 6 mo of EBF is likely to be warranted. In such
settings the nutritional quality of such foods is also likely to be
less than that of breast milk (Brown et al. 1998
,
Lutter et al. 1992
), making this a reasonable
suggestion. However, because the recommended length of EBF is important
for the interpretation of the Code, a universal recommendation is still
needed.
Replication of results is a cornerstone of scientific research
and calls for the results to be replicated prior to changing the
long-standing WHO recommendation are understandable
(Frongillo and Habicht 1997
). Ideally, replication
should be done in Africa or Asia so that the results can be generalized
more broadly outside of Latin America. However, differences in judgment
as to the level of evidence needed to some extent are inevitable as
illustrated by the fact that a number of Ministers of Health, the
American Academy of Pediatrics and UNICEF have changed their
recommendation.
As in any biological system, there is inherent variation in the length
of time EBF can satisfy infant energy and micronutrient requirements
and growth (Brown et al. 1998
, Lutter 1992
). Therefore, the development of a public health
recommendation involves not only scientific evidence but, just as
importantly, judgment and consensus about how best to describe the
inherent variability in the length of time EBF satisfies the energy,
micronutrient and growth needs of infants.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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2 It is unlikely that a public health
recommendation for length of EBF would ever extend beyond 6 mo of age
as this is the age when most infants can grab things and crawl, and
thus are exposed to environmental pathogens, apart from complementary
foods, which affects their risk of diarrhea. Delaying the introduction
of foods past 6 mo is likely to be in conflict with other cognitive and
social developmental needs of the infant.
3 The assumption that if energy requirements are
met by exclusive breastfeeding then the requirements for micronutrients
would be met as well should be explicitly tested in research assessing
the length of EBF for meeting infant nutrient requirements because
other nutrients such as iron and zinc may become limiting before
energy.
Manuscript received November 30, 1999. Initial review completed December 16, 1999. Revision accepted January 12, 2000.
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REFERENCES |
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TOPINTRODUCTIONThe biology of EBF...New scientific evidence on...Developing a public health...REFERENCES |
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1. Akre, J. (1989) Infant feeding: the physiological basis. Bull WHO 67(supplement): 1–108.
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3. Brown K. H., Dewey K. G. Relationships between maternal nutritional status and milk energy output of women in developing countries. Picciano M. F. Lonnerdal B. eds. Mechanisms Regulating Lactation and Infant Nutrient Utilization 1992:77-95 Wiley-Liss Inc New York.
4. Brown K. H., Dewey K. G., Allen L. H. Complementary feeding of young children in developing countries: A review of current scientific knowledge 1998 WHO/UNICEF. WHO Geneva, Switzerland.
5. Butte N. F. Energy requirements of infants. Eur. J. Clin. Nutr. 1996;50(1 Suppl):S24-S36
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7. Cohen R. J., Brown K. H., Canahuaiti J., Rivera L. L., Dewey K. G. Effects of age of introduction of complementary foods on infant breast milk intake, total energy intake, and growth: A randomized intervention study in Honduras. Lancet 1994;334:228-293
8. Cohen R. J., Landa L., Rivera A., Canahuati J., Brown K. H., Dewey K. G. Delaying the introduction of complementary foods until 6 months does not affect appetite or mothers report of food acceptance of breast-fed infants from 6 to 12 months of age in a low income, Honduras population. J. Nutr. 1995;125:2787-2793
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11. Dewey K. G., Peerson J. M., Brown K. H., Krebs N. F., Michaelsen K. F., Persson L. A., Salmenpera L., Whitehead R. G., Yeung D. L. Growth of breast-fed infants deviates from current reference data: a pooled analysis of U.S., Canadian, and European data sets. World Health Organization Working Group on Infant Growth. Pediatr. 1995;965:495-503
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13. Konis-Booher, P., Fishman, C., Parlato, M. & Roberts, A. (1990) Answering Key Questions: Recommendations from the Expert Meeting on Infant Feeding Practices. September 24–25: 1990. Academy for Educational Development, Washington, D.C.
14. Lutter, C. K. (1992) Recommended length of exclusive breast-feeding, age of introduction of complementary foods and the weanling dilemma. WHO/CDD/EDP92.5. Geneva, Switzerland.
15. Lutter C. K. Breastfeeding promotion: is its effectiveness supported by scientific evidence and global changes in breastfeeding behaviors?. Koletzo B. Michaelson K. eds. The Short- and Long-Term Effects of Breastfeeding on Infant Health In press Plenum Press New York, NY.
16. National Research Council. (1989) Recommended Dietary Allowances. 10th ed., National Academy of Sciences. Washington, D.C.
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Perez-Escamilla R., Cohen R. J., Brown K. H., Rivera L. L., Canahuati J., Dewey K. G. Maternal anthropometric status and lactation performance in a low-income Honduran population: Evidence for the role of infants. Am. J. Clin. Nutr. 1995;61:528-534
18. Prentice A. M., Paul A. A., Prentice A., Black A., Cole T., Whitehead R. Cross-cultural differences in lactational performance. Hamosh M. Goldman A. S. eds. Human Lactation 2: Maternal and Environmental Factors 1986:13-44 Plenum Press New York, NY.
19. Saint L., Maggiore P., Hartmann P. E. Yield and nutrient content of milk in eight women breast-feeding twins and one woman breast-feeding triplets. Br. J. Nutr. 1986;56:49-58[Medline]
20. Whitehead R. G., Paul A. A. Growth charts and the assessment of infant feeding practices in the western world and in developing countries. Early Hum. Dev. 1984;9:187-207[Medline]
21. WHO International Code of Marketing of Breast-milk Substitutes 1981 World Health Organization Geneva, Switzerland.
22. WHO Joint WHO/UNICEF Meeting on Infant and Young Child Feeding. Statement and Recommendations 1979 World Health Organization Geneva, Switzerland.
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