PEDIATRICS Vol. 99 No. 6 June 1997,
p. e5
Copyright ©1997 by the American Academy of Pediatrics
ELECTRONIC ARTICLE:
A Longitudinal Analysis of Infant Morbidity and the Extent of
Breastfeeding in the United States
Paula D. Scariati*,
Laurence M. Grummer-Strawn
, and
Sara Beck Fein§
From the * Epidemic Intelligence Service, Epidemiology Program
Office and Division of Nutrition and Physical Activity, National Center
for Chronic Disease Prevention and Health Promotion, Centers for
Disease Control and Prevention, Atlanta, Georgia; Division of
Nutrition and Physical Activity, National Center for Chronic Disease
Prevention and Health Promotion, Centers for Disease Control and
Prevention, Atlanta, Georgia; and the § Office of Scientific Analysis
and Support, Center for Food Safety and Applied Nutrition, Food and
Drug Administration, Washington, DC.
ABSTRACT
- INTRODUCTION
- METHODS
- RESULTS
- DISCUSSION
- FOOTNOTES
- ACKNOWLEDGMENTS
- REFERENCES
ABSTRACT 
Background. Studies on the health
benefits of breastfeeding in developed countries have shown conflicting
results. These studies often fail to account for confounding, reverse
causality, and dose-response effects. We addressed these issues in
analyzing longitudinal data to determine if breastfeeding protects US
infants from developing diarrhea and ear infections.
Methods. Mothers participating in a mail panel provided
information on their infants at ages 2, 3, 4, 5, 6, and 7 months. Infants were classified as exclusively breastfed; high, middle, or low
mixed breast- and formula-fed; or exclusively formula-fed. Diarrhea and
ear infection diagnoses were based on mothers' reports. Infant age and
gender; other liquid and solid intake; maternal education, occupation,
and smoking; household size; family income; and day care use were
adjusted for in the full models.
Results. The risk of developing either diarrhea or ear
infection increased as the amount of breast milk an infant received decreased. In the full models, the risk for diarrhea remained significant only in infants who received no breast milk compared with
those who received only breast milk (odds ratio = 1.8); the risk
for ear infection remained significant in the low mixed feeding group
(odds ratio = 1.6) and among infants receiving no breast milk
compared with those who received only breast milk (odds ratio = 1.7).
Conclusions. Breastfeeding protects US infants against the
development of diarrhea and ear infection. Breastfeeding does not have
to be exclusive to confer this benefit. In fact, protection is afforded
in a dose-response manner. The more breast milk an infant receives in
the first 6 months of life, the less likely that he or she will develop
diarrhea or ear infection. longitudinal analysis, diarrhea,
ear infection, breastfeeding.
INTRODUCTION
Does breastfeeding protect against infection? In developing
countries, the answer clearly is yes.1 However, in
industrialized countries the findings are mixed. Numerous
nonprospective studies of industrialized populations in the literature
examine the association between breastfeeding and infectious disease;
many report a protective effect5 whereas others report
little or no effect at all.13,14 Prospective studies show
similarly conflicting findings.15 A 1986 review of the
literature concluded that breastfeeding "has at most a minimal
protective effect [against infection] in industrialized countries."26
The conflicting results have been attributed to flawed
methodologies.20,23,26 Specific criticisms include
failure to (1) collect data prospectively at frequent intervals; (2)
control for known confounding variables such as day care, infant age, and indicators of socioeconomic status; (3) clearly define feeding and
outcome variables; (4) apply appropriate statistical strategies to a
population in which both feeding and exposure to infectious agents
change over time; and (5) account for small samples with the potential
for unspecified biases.
The objective of our study was to determine if breastfeeding protects
US infants against the development of diarrhea and ear infection. If
the answer was affirmative, we also wanted to know whether the
breastfeeding has to be exclusive to confer these benefits.
METHODS
Sampling Frame
The Infant Feeding Practices Study was a panel study of US
mother-infant pairs followed from late pregnancy through the infant's first year. The Food and Drug Administration conducted the study between 1993 and 1994. The agency used as the sampling frame a consumer
mail panel which yielded a set of households in which someone had
agreed to respond to questionnaires. The panel included approximately
500 000 households, and the contractors attempted to maintain
(compared with US Census data) representativeness on five
characteristics: geographic region, annual income, population density,
household size, and age. Members of the panel were recruited in a
variety of ways: recommendation from other panel members, notices in
places likely to attract the type of people needed, and lists compiled
by companies who specialize in finding particular types of people.
Prenatal intake questionnaires were sent to 3155 households identified
as including a pregnant women. All infants enrolled in this study were
born between March and October 1993.
Exclusion Criteria
Subjects were considered ineligible for the study at the time of
the prenatal questionnaire if the expected due date was more than 3 months away. After the prenatal questionnaire was administered, subjects were ineligible for the study if the infant weighed less than
5 pounds at birth, there were multiple infants, medical problems prevented the mother from feeding her infant for more than 1 week, the
infant stayed in the intensive care unit for more than 3 days, the
infant had medical problems that affected feeding, the mother or infant
died at any time during the data collection period, or the infant was
born too early for the neonatal questionnaire to be administered on
time. Five hundred forty women were ineligible, yielding a sample base
of 2615 mother-infant pairs.
Data Collection
The Infant Feeding Practices Study was a series of 11 questionnaires administered by mail beginning when the mother was
approximately 6 months pregnant and continuing until the infant was 1 year old. Infant feeding and health status information were collected
at months 2, 3, 4, 5, 6, and 7 (ie, when the infant was 2, 3, 4, 5, 6, and 7 months old). Information on smoking status and day care use was
collected at months 3 and 6. An additional demographic questionnaire
collected information on education, employment, household size, and
income.
Nonresponse
A woman was considered a nonrespondent if she failed to complete
the first (prenatal) or second (birth screener) questionnaire or if she
failed to complete at least one of the first two questionnaires sent
after the infant's birth (n = 812). We did not eliminate a mother
from the study for failure to complete a subsequent questionnaire. The
response rate was 69% (1803/2615).
For this analysis, we excluded women who failed to complete the
demographic questionnaire (n = 60), which left 1743 mother-infant pairs. In any given month, we also excluded infants who received neither breast milk nor formula.
There was a slight attrition in the number of questionnaires completed
at each successive month. We compared the demographic characteristics
of mothers completing all the questionnaires between months 2 and 7 with those missing at least one questionnaire. The two groups were
similar regarding household size, infant gender, and income. They were
different concerning education and employment. Mothers with a higher
level of education were more likely than less educated mothers to
complete all the questionnaires. Similarly, homemakers and professional
women were more likely to complete all the questionnaires.
Population Characteristics
To better understand the characteristics of our sample, we
compared them with a nationally representative population of mothers participating in the National Maternal and Infant Health
Survey.31 In comparison, our cohort of mothers was
more likely to belong to middle- and upper-income groups; to be older,
white, and married; and to have taken a prenatal class. They were also
less likely to drink alcohol or smoke.
Classification of Predictor and Outcome Variables
Each month, the mother reported the number of times over the
past 7 days that her infant received breast milk, formula, or both.
Using this information, we created five feeding categories based on the
percentage of breastfeedings an infant received: breast milk only
(100% of feedings were breast milk), high mixed (89% to 99% of
feedings were breast milk), middle mixed (58% to 88% of feedings were
breast milk), low mixed (1% to 57% of feedings were breast milk), and
formula only (0% of feedings were breast milk). The cutoffs for the
mixed feeding categories (ie, high, middle, and low) were defined by
dividing the mixed-feeding group into terciles. Table 1
lists the sample size for each breastfeeding group and the infant's
age in months.
|
Table 1.
Sample Size by Age of Child and Feeding Category in the Preceding Month
[View Table]
|
Each month, the mother also reported whether her infant had experienced
diarrhea or an ear infection in the preceding 2 weeks. Diarrhea was
defined for the mother as three or more watery or semiwatery stools in
a 24-hour period. Before answering this question, the mother was asked
to describe the infant's usual stool. We believe this gave her a
reference by which to distinguish between normally loose stools and
diarrhea. Ear infection was not predefined.
Confounding Variables
Each month, the mother reported the number of times in the past
7 days her infant received other liquids (cow's milk, other milk,
other dairy products, and fruit juice) or solids (baby cereal, other
cereals, fruit, vegetables, meat, peanut butter, eggs, and sweets). All
analyses, including the crude models, were adjusted for whether or not
the infant received in the previous month any other liquids and any
solids.a The infant's intake of other
liquids and solids was adjusted separately to allow us to examine the
formula-breast milk differential independent of any other intake the
infant received. We also adjusted all models for the infant's age as a
categorical variable.
In the full models, we also adjusted for infant gender; maternal
education, occupation, and smoking pattern; household size and income;
and day care use (Table 2). Maternal education, maternal occupation, household size, and household income are socioeconomic indicators that have known associations with both breastfeeding and
infectious disease. Day care use increases the risk of infection because it increases exposure to infectious agents, and it decreases breastfeeding because the infant is physically separated from its
mother. Maternal smoking is associated with increased risk of
infectious disease as well as decreased lactational
capacity,32 and it may be a marker of maternal health
behaviors. Data on day care and maternal smoking were collected only in
months 3 and 6. Therefore, for outcomes in month 4, the day care and
smoking data were imputed from responses given in month 3; for outcomes in months 5 and 7, the day care and smoking data were imputed from
responses given in month 6.
|
Table 2.
Confounding Variables Used in Multivariate Analysis
[View Table]
|
Analysis
We linked infection in any given month with feeding for the
preceding month. Thus, infection in month 3 was linked to feeding in
month 2; infection in month 4 was linked to feeding in month 3, and so
on. This lagged association allowed us to rule out the possibility of
reverse causality (ie, the type of milk given to an infant changes in
response to illness rather than the illness results from the type of
milk given) by ensuring that a reported illness occurred after a
specified type of feeding. This information then was aggregated across
all the groups so we could examine the effect of the previous
month's feeding on diarrhea and ear infection.
We used logistic regression to model the effects of covariates on the
odds of experiencing diarrhea and ear infections. Because several
months of data were included for each child, it was necessary to
account for the correlation of the data from 1 month to the next in the
estimation of the regression models. To do this, we used the
Generalized Estimating Equations approach33,34 and assumed that the correlation structure of the data was best captured by
stationary 1-dependence. This correlation structure assumes that there
is a constant degree of correlation between any two adjacent months of
data for a single child (eg, outcomes in month 3 are correlated with
outcomes in month 4 to the same extent that outcomes in month 4 are
correlated with outcomes in month 5, and so on). We experimented with
other correlation structures and found little change in the parameter
estimates or standard errors. We performed the analysis using the
Statistical Package for Interactive Data Analysis (SPIDA), version 6 (Statistical Computing Laboratory, New South Whales, Australia).
RESULTS
An analysis of our baseline data indicated that anywhere from
5.4% to 11.4% of our infants reportedly experienced diarrhea between
2 and 7 months of age; 6.8% to 13.2% experienced an ear infection
(Table 3). In the crude model, the association between the
percentage of breastfeedings and the development of diarrhea showed a
dose-response effect (Fig 1). Specifically, when each feeding group was compared with infants who received breast milk only
(referent), there was a small but steady increase in the risk of
developing diarrhea as the amount of breast milk an infant received
decreased. This was significant among low mixed
(P = .02) and formula only
(P < .001) infants. When we adjusted this model
for confounders, the dose-response remained apparent, although its
magnitude diminished and the effect remained significant only among
infants receiving no breast milk (P < .001).
|
Table 3.
Percentage of Infants 2 to 7 Months of Age Reported as Experiencing
Diarrhea or Ear Infection, by Feeding Category in the Preceding Month
[View Table]
|
Association between diarrhea and feeding in preceding 1 month.
Fig. 1.
Asterisks indicate P < .05 relative to
breast-milk-only group. Crude analyses takes into account infant's age
and intake of other liquids and solids for the preceding month.
Adjusted analyses take into account infant's age, gender, and intake
of other liquids and solids the previous month; maternal education,
occupation, and smoking pattern; household size and income; and day
care use.
[View Larger Version of this Image (20K GIF file)]
A dose-response relationship also emerged when we assessed the effect
of feeding on ear infections (Fig 2). Again, as the amount
of breast milk an infant received decreased, relative to the referent
group, the risk of developing an ear infection steadily increased, up
to an 80% increased risk among low mixed (P = .003) or formula only (P < .001) infants. When
we adjusted the model, the magnitude of the effect diminished but the
associations in both the low mixed (P = .02) and
formula only (P < .001) groups remained
significant.
Association between ear infection and feeding in preceding 1 month.
Fig. 2.
Asterisks indicate P < .05 relative to
breast-milk-only group. Crude analyses takes into account infant's age
and intake of other liquids and solids for the preceding month.
Adjusted analyses take into account infant's age, gender, and intake
of other liquids and solids the previous month; maternal education,
occupation, and smoking pattern; household size and income; and day
care use.
[View Larger Version of this Image (21K GIF file)]
DISCUSSION
We conclude that breastfeeding protects US infants against the
development of diarrhea and ear infection. Exclusive breastfeeding is
not crucial to confer this benefit. In fact, protection is afforded in
a dose-response manner.
In looking at the relationship between feeding and diarrhea (after
accounting for confounders), we found the odds ratios across feeding
groups showed a steadily increasing risk of diarrhea as the relative
amount of breast milk decreased. A similar pattern of protection was
seen for ear infections. When compared with exclusively breastfed
infants, infants who received formula only had an 80% increase in
their risk of developing diarrhea and a 70% increase in their risk of
developing an ear infection.
We view these findings in light of the limitations of this study.
Because mothers responded via a mailed survey, some misclassification of diarrhea or ear infections may have occurred. Furthermore, the
normally loose stools of breastfed infants may have been misreported as
diarrhea. Under both of these circumstances, the bias created would
weaken the strength of our association. Thus, our results may
underestimate the true magnitude of the relationship between infant
feeding and diarrhea or ear infections. Second, feeding choices reflect
inherent differences between mothers. We addressed this limitation by
controlling for a wide variety of sociodemographic characteristics, but
other characteristics that were not measured could confound our
results. Third, mothers who participate in mail panel surveys may
differ from the general population. As we noted earlier, our study
population was of a higher socioeconomic status than the general
population. This difference should have also weakened the strength of
our association, because we expected the benefits of breastfeeding to
be harder to demonstrate in high-socioeconomic status groups. Finally,
the sample size of this study did not allow us to examine the effect of
feeding infants a small proportion of breast milk relative to formula
(eg, <20%). This group was small because it is physiologically
difficult for a mother to maintain small numbers of breastfeedings over
prolonged periods.
A notable strength of this study is its methodology. By using
longitudinal data, we were able to examine infectious disease outcomes
in relation to the feeding pattern that immediately preceded them.
Because the data were collected month by month, it was possible to
obtain specific data on supplemental foods as well as the number of
formula feedings and breastfeedings, thus allowing a very precise definition of feeding patterns unaffected by recall bias. Appropriate statistical methods were used to account for the longitudinal nature of
the data.
It is our hope that the three main points of this study will serve as
tools for the education of pregnant and lactating women in the US.
First, breast milk provides protection against selected diseases. This
adage is by no means new, but past evidence for protection against
infectious disease in developed countries has been less than
adequate.13,14,18,20,24 In the US, where only 53% of
women initiate breastfeeding,35 it is a message that
deserves renewed attention and support. Second, supplementing breastfeedings with small amounts of formula does not eliminate the
protection afforded by breast milk. Clearly, this is not meant to
discourage mothers from practicing exclusive breastfeeding, but, in a
society where the mother has to meet many responsibilities in addition
to feeding her infant, exclusive breastfeeding may not always be
practical. Finally, breastfeeding is not an all-or-none phenomenon; the
more breast milk an infant receives in the first 6 months of life, the
better.
FOOTNOTES
a Additional analyses controlling for the number
of feedings of liquids or solids did not substantively alter our
results.
Received for publication Sept 5, 1996; accepted Dec 23, 1996.
Reprint requests to (P.S.) Centers for Disease Control and
Prevention, Mailstop K-25, Division of Nutrition and Physical Activity,
4770 Buford Highway, Atlanta, GA 30341-3724.
ACKNOWLEDGMENTS
The authors thank Drs David Kleinbaum and Amrik Shah for sharing
their expertise and advice concerning analyses of longitudinal data. We
also thank Dr Kelley Scanlon for her careful review of this manuscript.
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