Infant feeding patterns and risks of death and hospitalization in the first half of infancy: Multicentre cohort study

Article (PDF Available)inBulletin of the World Health Organisation 83(6):418-26 · June 2005with53 Reads
Source: PubMed
Abstract
To determine the association of different feeding patterns for infants (exclusive breastfeeding, predominant breastfeeding, partial breastfeeding and no breastfeeding) with mortality and hospital admissions during the first half of infancy. This paper is based on a secondary analysis of data from a multicentre randomized controlled trial on immunization-linked vitamin A supplementation. Altogether, 9424 infants and their mothers (2919 in Ghana, 4000 in India and 2505 in Peru) were enrolled when infants were 18-42 days old in two urban slums in New Delhi, India, a periurban shanty town in Lima, Peru, and 37 villages in the Kintampo district of Ghana. Mother-infant pairs were visited at home every 4 weeks from the time the infant received the first dose of oral polio vaccine and diphtheria-pertussis-tetanus at the age of 6 weeks in Ghana and India and at the age of 10 weeks in Peru. At each visit, mothers were queried about what they had offered their infant to eat or drink during the past week. Information was also collected on hospital admissions and deaths occurring between the ages of 6 weeks and 6 months. The main outcome measures were all-cause mortality, diarrhoea-specific mortality, mortality caused by acute lower respiratory infections, and hospital admissions. There was no significant difference in the risk of death between children who were exclusively breastfed and those who were predominantly breastfed (adjusted hazard ratio (HR) = 1.46; 95% confidence interval (CI) = 0.75-2.86). Non-breastfed infants had a higher risk of dying when compared with those who had been predominantly breastfed (HR = 10.5; 95% CI = 5.0-22.0; P < 0.001) as did partially breastfed infants (HR = 2.46; 95% CI = 1.44-4.18; P = 0.001). There are two major implications of these findings. First, the extremely high risks of infant mortality associated with not being breastfed need to be taken into account when informing HIV-infected mothers about options for feeding their infants. Second, our finding that the risks of death are similar for infants who are predominantly breastfed and those who are exclusively breastfed suggests that in settings where rates of predominant breastfeeding are already high, promotion efforts should focus on sustaining these high rates rather than on attempting to achieve a shift from predominant breastfeeding to exclusive breastfeeding.
418
Bulletin of the World Health Organization
| June 2005, 83 (6)
Objective To determine the association of different feeding patterns for infants (exclusive breastfeeding, predominant breastfeeding,
partial breastfeeding and no breastfeeding) with mortality and hospital admissions during the first half of infancy.
Methods This paper is based on a secondary analysis of data from a multicentre randomized controlled trial on immunization-linked
vitamin A supplementation. Altogether, 9424 infants and their mothers (2919 in Ghana, 4000 in India and 2505 in Peru) were enrolled
when infants were 18–42 days old in two urban slums in New Delhi, India, a periurban shanty town in Lima, Peru, and 37 villages in the
Kintampo district of Ghana. Mother–infant pairs were visited at home every 4 weeks from the time the infant received the first dose of
oral polio vaccine and diphtheria–pertussis–tetanus at the age of 6 weeks in Ghana and India and at the age of 10 weeks in Peru. At
each visit, mothers were queried about what they had offered their infant to eat or drink during the past week. Information was also
collected on hospital admissions and deaths occurring between the ages of 6 weeks and 6 months. The main outcome measures were
all-cause mortality, diarrhoea-specific mortality, mortality caused by acute lower respiratory infections, and hospital admissions.
Findings There was no significant difference in the risk of death between children who were exclusively breastfed and those who
were predominantly breastfed (adjusted hazard ratio (HR) = 1.46; 95% confidence interval (CI) = 0.75–2.86). Non-breastfed infants
had a higher risk of dying when compared with those who had been predominantly breastfed (HR = 10.5; 95% CI = 5.0–22.0;
P
< 0.001) as did partially breastfed infants (HR = 2.46; 95% CI = 1.44–4.18;
P
= 0.001).
Conclusion There are two major implications of these findings. First, the extremely high risks of infant mortality associated with not
being breastfed need to be taken into account when informing HIV-infected mothers about options for feeding their infants. Second,
our finding that the risks of death are similar for infants who are predominantly breastfed and those who are exclusively breastfed
suggests that in settings where rates of predominant breastfeeding are already high, promotion efforts should focus on sustaining
these high rates rather than on attempting to achieve a shift from predominant breastfeeding to exclusive breastfeeding.
Keywords Infant nutrition; Feeding behavior; Breast feeding; Infant mortality; Cause of death; Diarrhea/mortality; Respiratory tract
infections/mortality; Hospitalization; Infant; Cohort studies; Multicenter studies; Ghana; India; Peru (
source: MeSH, NLM
).
Mots clés Nutrition nourrisson; Comportement alimentaire; Allaitement au sein; Mortalité nourrisson; Cause décès; Diarrhée/mortalité;
Voies aériennes supérieures, Infection/mortalité; Hospitalisation; Nourrisson; Etude cohorte; Etude multicentrique, Ghana; Inde; Pérou
(
source: MeSH, INSERM
).
Palabras clave Nutrición infantil; Alimentos infantiles: Conducta alimentaria; Lactancia materna; Mortalidad infantil; Causa de
muerte; Diarrea/mortalidad; Infecciones del tracto respiratorio/mortalidad; Hospitalización; Lactante; Estudios de cohortes; Estudios
multicéntricos; Ghana; India; Perú (
fuente: DeCS, BIREME
).
Bulletin of the World Health Organization 2005;83:418-426.
Voir page 424 le résumé en français. En la página 425 figura un resumen en español.
Infant feeding patterns and risks of death and hospitalization
in the first half of infancy: multicentre cohort study
Rajiv Bahl,
1
Chris Frost,
2
Betty R. Kirkwood,
3
Karen Edmond,
4
Jose Martines,
5
Nita Bhandari,
6
& Paul Arthur
7
1
Medical Officer, Department of Child and Adolescent Health and Development, World Health Organization, Geneva, Switzerland.
2
Reader in Medical Statistics, Department of Epidemiology and Population Health, London School of Hygiene and Tropical Medicine, London, England.
3
Professor of Epidemiology and International Health, Department of Epidemiology and Population Health, London School of Hygiene and Tropical Medicine, Keppel
Street, London WC1E 7HT, England (email: betty.kirkwood@lshtm.ac.uk). Correspondence should be sent to this author.
4
Research Fellow in Paediatric Epidemiology, Department of Epidemiology and Population Health, London School of Hygiene and Tropical Medicine, London, England.
5
Coordinator, Newborn and Infant Health Team, Department of Child and Adolescent Health and Development, World Health Organization, Geneva, Switzerland.
6
Scientist, Centre for Diarrhoeal Disease and Nutrition Research, Department of Paediatrics, All India Institute of Medical Sciences, New Delhi, India.
7
Director (deceased), Kintampo Health Research Centre, Ghana Health Service, PO Box 200, Kintampo, Brong Ahafo Region, Ghana.
Ref. No.
04-018143
(
Submitted: 17 September 2004 – Final revised version received: 4 February 2005 – Accepted: 7 February 2005
)
Introduction
The recognition that human immunodeficiency virus (HIV)
is transmitted through breast milk has resulted in the need to
inform all women infected with HIV about this risk and to rec-
ommend that they avoid breastfeeding if replacement feeding is
.425
acceptable, feasible, affordable, safe and sustainable; alterna-
tively, they should be advised to breastfeed exclusively but to
stop as early as possible (1). The advice to breastfeed exclu-
sively is based on the finding that infants who are exclusively
or predominantly breastfed have a lower risk of dying from
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| June 2005, 83 (6)
Research
Rajiv Bahl et al. Infant feeding patterns and risks of death
common childhood infections than those who are partially or
completely weaned (2) and that exclusive breastfeeding may
carry a lower risk of HIV transmission than partial breastfeed-
ing (3, 4). The most important elements of the information
given to HIV-infected mothers in order to help them make an
informed decision on infant feeding concern the risk of HIV
transmission through breastfeeding and the risk of mortality
and severe morbidity caused by infectious diseases that is as-
sociated with avoidance of all breastfeeding.
A pooled analysis of data from six developing countries
has quantified the effect of an infant never being breastfed
on the risk of mortality caused by infectious disease (5). An
important limitation of this pooled analysis was that most of
the studies did not supply sufficient information on patterns of
breastfeeding, such as whether a child was exclusively breastfed,
predominantly breastfed or partially breastfed. For our pur-
poses, exclusive breastfeeding means that a child is fed only
breast milk; predominant breastfeeding means that the infant
may also be given some non-breast-milk liquids but not animal
milk, formula or solids; partial breastfeeding means that the
infant may be given animal milk, formula or solids in addition
to breast milk. In the absence of this information, the pooled
analysis could not compare the effect of no breastfeeding with
different breastfeeding patterns, particularly with exclusive
breastfeeding, which is the recommendation for the first 6
months of life (6). A subsequent study in Bangladesh attempted
to address this issue but included only a small number of non-
breastfed infants and consequently grouped them with those
who had been partially breastfed (7).
Exclusive breastfeeding during the first 6 months of life
has been identified as one of the key interventions for reduc-
ing childhood deaths in a group of articles on child survival
published in the
Lancet (8). Although 90% infants in the 42
countries that accounted for 90% of childhood deaths world
-
wide in 2000 are estimated to be breastfed up until the age of
12 months, demographic surveys show that only 39% of infants
aged < 6 months are exclusively breastfed (range = 1–84%) (
8).
Studies conducted with more rigour report even lower preva-
lences of exclusive breastfeeding, probably because many
infants who are predominantly breastfed have been classi
-
fied as exclusively breastfed during demographic surveys (7,
9–13). Randomized trials in different parts of the world have
demonstrated the feasibility of improving breastfeeding rates
through community-based interventions (
9–11). While the
interventions resulted in some infants shifting from partial
breastfeeding to exclusive breastfeeding, the largest move to
exclusive breastfeeding probably occurred among those infants
who had been predominantly breastfed (9–11). In India, for
example, 31% more infants were exclusively breastfed at 3
months of age in the intervention group when compared with
the control group. Correspondingly, when compared with the
control group 21% fewer infants in the intervention group
were predominantly breastfed, 9% fewer infants were partially
breastfed, and 1% fewer infants were not breastfed (9). These
studies were, however, too small to assess the effect of the inter
-
vention on mortality. Estimates of the proportion of deaths that
can be prevented by such programmes require ascertainment
of the effect of exclusive breastfeeding on the overall risk of
mortality and the cause-specific risk of mortality from infec-
tious disease when compared with predominant breastfeeding
and partial breastfeeding.
Two questions therefore remain. First, among children
who are not breastfed, what is the excess risk of overall mortality,
cause-specific mortality and severe morbidity during the first 6
months of life compared with children who are exclusively or
predominantly breastfed? Second, what is the effect of partial
breastfeeding on the same outcomes when compared with ex-
clusive or predominant breastfeeding?
To answer these questions we performed a secondary
analysis of data from a multicentre randomized controlled trial
on immunization-linked vitamin A supplementation; the
results related to vitamin A supplementation have been pub-
lished earlier (14). The findings of this secondary analysis are
presented in this paper.
Methods
A detailed description of the study sites and methods has been
published earlier (14). Methods relating to secondary analysis of
the association between infant feeding patterns and the risk of
overall mortality, cause-specific mortality and severe morbidity
are described here.
Setting
The study took place in Ghana, India and Peru. Participants
were enrolled from two urban slums in New Delhi, a periurban
shanty town in Lima and from 37 villages in the Kintampo dis
-
trict of Ghana. Initiation of breastfeeding was almost universal
within the first few days after birth; and in all regions more
than 94% of the infants were receiving breast milk after the
age of 9 months. All study sites were characterized by high rates
of infant morbidity, especially from diarrhoea and respiratory
infections. In Kintampo, malaria was also common. Stunting
(defined as length for age < –2 z scores) and wasting (weight
for length < –2 z scores) at 12 months of age were common
in New Delhi (42% of children classed as stunted and 6% as
having wasting) and Kintampo (32% classed as stunted and
4% as having wasting), but less so in Lima (10% classed as
stunted and 0.7% as having wasting).
Between January 1995 and June 1997, 9424 mother–
infant pairs were enrolled when the infants were 18–24 days
old; there were 2919 pairs in Ghana, 4000 in India and 2505
in Peru. Follow-up lasted until the infant was 12 months old,
except among the last 806 pairs in Ghana and 522 in Lima
whose follow-up was stopped some time after 6 months old in
order to adhere to the study’s timeline. This truncation does
not affect the results presented in this paper, since the period
of interest is from enrolment to the age of 6 months.
Data collection
At the time of enrolment, information was collected from
each mother–infant pair on socioeconomic and environmental
variables, such as the mothers educational level, place of defeca
-
tion, where the household got its water, the number of family
members, amount of household sleeping space (that is, the total
number of family members who had slept in the house the
previous night and the number of rooms available for sleep-
ing), and the type of house. Information was also collected on
maternal age and the infant’s sex and birth order. All infants
were also weighed.
Beginning from the age when the infant was given the
first dose of oral polio vaccine and diphtheria–pertussis–tetanus
vaccine (at 6 weeks in Ghana and India and 10 weeks in Peru),
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Infant feeding patterns and risks of death Rajiv Bahl et al.
each enrolled pair was visited at home by a trained field worker
every 4 weeks. At each visit, mothers were queried about what
they had offered their child to eat or drink during the past week.
After the mothers unprompted response was recorded, she was
asked whether she had offered her own breast milk, breast milk
from a wet nurse, animal milk, infant formula, other fluids or
solid foods at any time during the week.
Information was also collected on hospital admissions
and deaths. The primary cause of death was ascertained from
hospital records or verbal autopsy using forms developed by
Johns Hopkins University, the London School of Hygiene and
Tropical Medicine, and the WHO Verbal Autopsy Validation
Collaborative Group. Verbal autopsies were conducted within 6
weeks of an infant’s death through interviews with caregivers
at their home. Three paediatricians at each study site indepen
-
dently reviewed the verbal autopsy forms to ascertain the pri
-
mary cause of death; any differences of opinion were discussed,
and agreement was reached through consensus. The primary
causes of hospitalizations were determined from hospital re
-
cords or discharge papers.
Statistical analysis and definitions
Exclusive breastfeeding was defined as an infant being fed only
breast milk and nothing else, not even water, with the exception
of vitamin supplements and prescribed medicines. Predomi
-
nant breastfeeding was defined as an infant being fed breast
milk along with some other non-breast-milk fluids but not
animal milk, infant formula or solids. Infants who were offered
breast milk and animal milk, infant formula or solids were con
-
sidered to be partially breastfed. These definitions are consistent
with WHO definitions for breastfeeding patterns (
6).
Infants were classified by the exposure variable (breast
-
feeding status) as exclusively breastfed, predominantly breast
-
fed, partially breastfed or not breastfed at the 6 week, 10 week,
14 week, 18 week and 22 week follow-up visits. If breastfeeding
status was recorded as missing at a particular visit it was inferred
to be the same as that at the immediately preceding visit. If
breastfeeding status had also been recorded as missing at the
preceding visit, then no further extrapolation was carried out.
Periods of time during which breastfeeding status was missing
were omitted from all analyses.
The outcome variables were all-cause deaths, deaths due
to acute lower respiratory tract infections (ALRI), diarrhoea-
specific deaths, all-cause hospitalizations, ALRI-specific hos
-
pitalizations and diarrhoea-specific hospitalizations occurring
between the ages of 6 weeks and 26 weeks.
All analyses were carried out using Stata software, version
8.2. Breastfeeding status at each follow-up visit was related
to mortality in the following period using Coxs models with
time-dependent covariates stratified by country. Such models
allow hazard ratios to be estimated while also allowing the
underlying risk of death to vary during the follow-up period.
Breastfeeding status at each follow-up visit was also related to
the risk of hospitalization in the following period using Poisson
models with (log) length of period as an offset. Such models
allow incidence ratios to be estimated. The models included
the period and site and their interactions as covariates in order
to allow for changes in risk over time by site. They were fitted
using a generalized estimating equation framework in order to
allow for potential non-independence of hospital admissions in
cases in which children were admitted more than once; robust
standard errors are reported.
We included as covariates those potential confounders
that have been previously reported to be associated with risk
of mortality and morbidity and possibly with infant feeding
patterns. These potential confounders were the infant’s sex,
twin status, birth order and weight at enrolment (as a marker
of birth weight), mother’s educational level, place of defeca
-
tion and household water supply. Randomization to receive
vitamin A supplementation or placebo was not considered to be
a confounder because it was neither associated with mortality
or hospitalization between the ages of 6 weeks and 26 weeks
nor with patterns of feeding.
The primary comparisons were made between being
exclusively breastfed and predominantly breastfed, between not
being breastfed and being predominantly breastfed, and be-
tween being partially breastfed and predominantly breastfed.
The group of infants who had been predominantly breastfed
was considered to be the reference group because it was sub-
stantially larger than the exclusive breastfeeding group and
therefore was likely to yield more robust results.
The study was approved by the appropriate ethics review
committees of all participating institutions and the WHO
Ethics Review Board.
Findings
Of the 9424 infants enrolled in the study, 9200 infants (2870
in Ghana, 3921 in India and 2409 in Peru) received their first
dose of vitamin A or placebo and their first diphtheria–per-
tussis–tetanus and polio vaccinations; these were given at the
age of 6 weeks in India and Ghana and 10 weeks in Peru (12).
Among these 9200 infants, 206 (2.2%) were not available at
the 26-week visit, and 118 had died between the age of 6 weeks
and 6 months.
Among the same 9200 infants, information on infant
feeding practices was available for 94.1% at the 6-week visit
(for Ghana and India only); information was available for
97.4% of infants at the 10-week visit, 96.2% at the 14-week
visit, 94.3% at the 18-week visit and 92.1% at the 22-week
visit. Information on feeding at either of the two visits im-
mediately preceding death was not available for 14 of the 118
infants who died.
Feeding patterns
In Ghana and India the prevalence of exclusive breastfeeding
was about 21% (568/2649 in Ghana; 788/3738 in India) at 6
weeks; this fell to about 3–4 % (73/2603 in Ghana; 138/3557
in India) at the 22-week visit. The prevalence of exclusive breast
-
feeding was higher in Peru; it was about 44% (1022/2315) at
the 10-week visit and 33% (766/2311) at the 22-week visit.
The most common feeding pattern in Ghana was pre-
dominant breastfeeding from the age of 6 weeks to the age of
6 months. In India the most common pattern at 6 weeks was
predominant breastfeeding, but partial breastfeeding became
the most prevalent pattern after the age of 14 weeks. In Peru
exclusive breastfeeding was the most common feeding pattern
from the ages of 10 weeks to 18 weeks, but partial breastfeed-
ing had become the most prevalent pattern by the age of 22
weeks (Table 1).
Overall, of the 3264 infant–years of follow-up between
the age of 6 weeks and 26 weeks, predominant breastfeeding
was the most common feeding pattern (48.6% of total follow-
up), followed by partial breastfeeding (31.0%), exclusive breast
-
feeding (18.5%) and no breastfeeding (1.9%).
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Rajiv Bahl et al. Infant feeding patterns and risks of death
the 95% confidence interval for the hazard ratio for ALRI just
includes 1 (P = 0.004 for diarrhoea-specific mortality and P =
0.063 for ALRI-specific mortality).
Feeding patterns and hospital admissions
Table 5 shows that there were no significant differences in the
risk of hospitalization between infants who were exclusively
breastfed and those who were predominantly breastfed or be-
tween those who were partially breastfed and those who were
predominantly breastfed. However, non-breastfed infants were
at a substantially higher risk of all-cause hospitalization (inci-
dence rate ratio (IRR) = 3.39; 95% CI = 1.74–6.61; P < 0.001)
and diarrhoea-specific hospitalization (IRR = 5.59; 95% CI =
2.17–14.4; P < 0.001) when compared with infants who had
been predominantly breastfed. The risk of ALRI-specific hospi-
talization was also higher but was not statistically significant at
the 5% level (IRR = 2.50; 95% CI = 0.93–6.74; P = 0.069).
Discussion
Principal findings
The two main findings are, first, that the risks of death or hos-
pitalization associated with being predominantly breastfed were
not significantly different from those associated with being ex-
clusively breastfed. Second, infants who had not been breastfed
had a 10-fold higher risk of dying of any cause and a 3-fold
higher risk of being hospitalized for any cause when compared
with those who had been predominantly breastfed.
Strengths of the study and comparison with other
studies
This paper presents the findings on overall mortality and cause-
specific risks of mortality and hospitalization associated with
infant feeding patterns among children aged from 6 weeks to
6 months; these results came from a large multicentre study
that followed more than 9400 infants in three sites in Africa,
Asia and Latin America. Previously published mortality risks
associated with not being breastfed have mostly been based on
a comparison with any breastfeeding.
Table 1. Infant feeding patterns at age 6, 10, 14, 18 and 22 weeks, by site in Ghana, India and Peru. Values are number (%) of visits
to infants
Ghana India Peru
Age at Exclu- Predomi- Par- Not Exclu- Predomi- Par- Not Exclu- Predomi- Par- Not
visit sively nantly tially breast- sively nantly tially breast- sively nantly tially breast-
(weeks) breast- breastfed breast- fed breast- breastfed breast- fed breast- breastfed breast- fed
fed
a
fed fed fed fed fed
6 568 1984 94 3 788 1852 1054 44 NA
b
NA NA NA
(21.4) (74.9) (3.5) (0.1) (21.1) (49.5) (28.2) (1.2)
10 419 2291 84 3 577 1815 1382 78 1022 491 775 27
(15.0) (81.9) (3.0) (0.1) (15.0) (47.1) (35.9) (2.0) (44.1) (21.2) (33.5) (1.2)
14 303 2327 114 3 381 1609 1631 106 1187 425 728 36
(11.0) (84.7) (4.1) (0.1) (10.2) (43.2) (43.8) (2.8) (50.0) (17.9) (30.6) (1.5)
18 163 2391 112 3 225 1221 2083 133 1029 411 850 55
(6.1) (89.6) (4.2) (0.1) (6.1) (33.3) (56.9) (3.6) (43.9) (17.5) (36.2) (2.3)
22 73 2340 185 5 138 786 2446 187 766 417 1046 82
(2.8) (89.9) (7.1) (0.2) (3.9) (22.1) (68.8) (5.3) (33.1) (18.0) (45.3) (3.5)
a
A full explanation of the feeding categories can be found in the text.
b
NA = not available.
Causes of death
Table 2 and Table 3 show the distribution of deaths by age
and cause of death. Overall, infectious diseases accounted for
about three-quarters of all deaths occurring between the ages
of 6 weeks and 26 weeks, with the most common causes being
diarrhoea (accounting for 42% (40/95) of all deaths with known
cause) and ALRIs (accounting for 20% (19/95) of all deaths
with known cause). However, in Peru there were no diarrhoeal
deaths: acute respiratory infections, sepsis and meningitis ac-
counted for more than half the deaths with known causes (5/9)
(Table 2 and Table 3).
Mortality
There was no significant difference in the risk of death between
infants who had been predominantly breastfed and those who
had been exclusively breastfed (Table 4). Non-breastfed infants
were at a substantially higher risk of dying compared with
those who had been predominantly breastfed (adjusted hazard
ratio (HR) = 10.5; 95% confidence interval (CI) = 5.0–22.0;
P < 0.001). Partially breastfed infants were also at a signifi-
cantly higher risk of death compared with those who had been
predominantly breastfed (HR = 2.46; 95% CI = 1.44–4.18;
P = 0.001, Table 4).
In order to address reverse causality — that is, the pos
-
sibility of breastfeeding patterns changing because of a serious
illness that led to death we repeated the above analysis
excluding those deaths that occurred within 7 days of an as-
sessment of feeding practices. In this analysis, the effect sizes
remained unchanged (for non-breastfed infants HR = 10.7;
95% CI = 4.54–25.1; P < 0.001, and for partially breastfed
infants HR = 2.42; 95% CI = 1.31–4.49; P = 0.005).
Table 4 also shows that non-breastfed infants were at a
substantially greater risk of death when compared with pre-
dominantly breastfed infants, from both diarrhoea (HR = 8.96;
95% CI = 2.56–31.4;
P = 0.001) and ALRI (HR = 32.7; 95%
CI = 6.82–157.2; P<0.001). Partially breastfed infants also
had a greater risk of dying from both these causes, although
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Infant feeding patterns and risks of death Rajiv Bahl et al.
Table 2. Distribution of deaths occurring between 6 weeks and 26 weeks of age in Ghana, India and Peru by feeding pattern
Ghana India Peru
Age Exclu- Predomi- Par- Not Exclu- Predomi- Par- Not Exclu- Predomi- Par- Not
(weeks) sively nantly tially breast- sively nantly tially breast- sively nantly tially breast-
breast- breastfed breast- fed breast- breastfed breast- fed breast- breastfed breast- fed
fed
a
fed fed fed fed fed
6–10 1 5 0 0 1 5 9 0 NA
b
NA NA NA
10–14 1 4 0 1 2 2 11 3 4 0 3 0
14–18 1 4 0 1 0 2 5 3 0 0 1 0
18–22 0 3 0 1 1 1 3 2 0 1 2 0
22–26 1 10 1 0 0 1 5 1 1 0 1 0
Total
c
4 26 1 3 4 11 33 9 5 1 7 0
a
A full explanation of the feeding categories can be found in the text.
b
NA = not available.
c
Of the 118 deaths that occurred during this period, information on feeding could not be characterized for 14 infants (5 in Ghana, 7 India and 2 in Peru).
Table 3. Distribution of deaths occurring between 6 weeks and 26 weeks of age in Ghana, India and Peru for which information
about the preceding visit’s feeding category was available, by infant feeding pattern and primary cause of death
a
Ghana India Peru
Primary Exclu- Predomi- Par- Not Exclu- Predomi- Par- Not Exclu- Predomi- Par- Not
cause of sively nantly tially breast- sively nantly tially breast- sively nantly tially breast-
death breast- breastfed breast- fed breast- breastfed breast- fed breast- breastfed breast- fed
fed
b
fed fed fed fed fed
Diarrhoea 1 9 0 1 2 4 20 3 0 0 0 0
Acute lower 0 7 0 1 0 1 5 3 0 0 2 0
respiratory
tract infection
Sepsis or 2 2 0 0 0 1 1 0 1 0 2 0
meningitis
Malaria 0 3 0 0 0 0 0 0 0 0 0 0
Others 1 4 1 1 2 4 5 2 2 0 2 0
Unknown
c
0 1 0 0 0 1 2 1 2 1 1 0
Total 4 26 1 3 4 11 33 9 5 1 7 0
a
Of the 118 deaths that occurred during this period, information on feeding could not be characterized for 14 infants (5 in Ghana, 7 India and 2 in Peru).
b
A full explanation of the feeding categories can be found in the text.
c
Verbal autopsies to ascertain the cause of death could not be done for 3 deaths in India and 4 deaths in Peru. The cause of 1 death in Ghana and 1 in India was
classified as uncertain.
An earlier pooled analysis, by the WHO Collaborative
Study Team on the Role of Breastfeeding on the Prevention
of Infant Mortality, found point estimates of odds ratios for
an increased risk of death ranging from 2.5 to 4.2 at different
ages for children who had not been breastfed when compared
with those who had had any breastfeeding (5). The studies
included in the pooled analysis did not have sufficient infor
-
mation to examine the excess risk of death associated with not
breastfeeding when compared with exclusive or predominant
breastfeeding. Our study revealed that the risks associated with
not being breastfed when compared with being predominantly
(or exclusively) breastfed are considerably higher: the hazard
ratio was 10.5 with a 95% confidence interval ranging from
5.0 to 22.0.
Furthermore, these results are likely to be an underesti-
mate of the true protective effect of exclusive or predominant
breastfeeding during the first half of infancy: the design of
this study did not permit us to examine the effect of feeding
patterns during the first 6 weeks of life. The analysis by the
WHO Collaborative Study Team reported a higher protec
-
tive effect for any breastfeeding in the first 2 months of life
when compared with the effect of breastfeeding among older
infants (5).
The effect on diarrhoeal deaths among infants not being
breastfed was almost as strong as the effect on all-cause mor-
tality; the effect on ALRI was even stronger. These findings are
in contrast to those of previous studies, which have reported
stronger negative effects of not being breastfed on deaths due
to diarrhoea than those due to ALRI when compared with any
breastfeeding (
2, 5, 15, 16). In this study, not being breastfed
was associated with a higher risk of hospitalization due to diar-
rhoea than to ALRI.
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Rajiv Bahl et al. Infant feeding patterns and risks of death
Table 4. Effect of feeding pattern on risk of all-cause mortality, diarrhoea-specific mortality and acute lower respiratory infection-
specific mortality among infants aged 6–26 weeks in Ghana, India and Peru. All analyses stratified by site
All-cause mortality Diarrhoea-specific mortality ALRI-specific mortality
a
Feeding Infant– No. of Unadjusted Adjusted No. of Unadjusted Adjusted No. of Unadjusted Adjusted
pattern years of deaths hazard hazard deaths hazard hazard deaths hazard hazard
follow up ratio
b
ratio
c
ratio ratio
c
ratio ratio
c
Exclusively 603.7 13 1.37 1.46 3 1.32 1.36 0
breastfed
d
(0.70–2.68) (0.75–2.86) (0.36–4.84) (0.37–5.03)
Predomi- 1587.2 38 1.0 1.0 13 1.0 1.0 8 1.0 1.0
nantly
breastfed
Partially 1011.1 41 2.86 2.46 20 4.01 3.37 7 3.64 3.57
breastfed (1.69–4.85) (1.44–4.18) (1.77–9.09) (1.46–7.75) (0.97–13.6) (0.93–13.7)
Not 61.5 12 15.5 10.5 4 14.6 8.96 4 38.9 32.7
breastfed (7.51–32.2) (5.0–22.0) (4.28–49.5) (2.56–31.4) (8.37–180.4) (6.82–157.2)
a
ALRI = acute lower respiratory infection.
b
Values in parentheses are 95% confidence intervals.
c
Adjusted for infant’s weight at enrolment, sex, twin status, birth order, and mother’s educational level, place of defecation, and household water supply.
d
A full explanation of the feeding categories can be found in the text.
The increased risks of hospitalization associated with
partial breastfeeding and non-breastfeeding (compared with
predominant breastfeeding) were considerably lower than the
associated increased risks of dying; for partial breastfeeding
the increased risk of hospitalization was moderate and non-
significant. It should be noted that these are additional risks
on top of the risks associated with death. This suggests that
the more severe the outcome the more protective predominant
breastfeeding will be.
Limitations
Observational studies of breastfeeding and infant health may
be affected by a number of methodological problems includ
-
ing self-selection, reverse causality and confounding; these have
been described elsewhere (17–20). In this analysis, we addressed
confounding by adjusting for most of the important character
-
istics of the infants and maternal and household characteristics
known to be associated with infant mortality and morbidity or
with breastfeeding. We conducted an analysis that excluded
all deaths occurring within 7 days of any assessment of feeding
in order to examine the issue of reverse causality. Our analysis
showed that excluding these deaths did not alter the size of the
effects. Therefore, we found no evidence of reverse causality in
our dataset and have presented the overall analysis including
all deaths and hospitalizations.
The difference in the risks between different causes should
be interpreted with caution because all sites had a relatively
small proportion of non-breastfed infants, and Ghana and India
had small proportions of exclusively breastfed infants. The for
-
mer resulted in an imprecise estimation of the mortality risk of
non-breastfed infants (CI = 5 to 22 times), and the latter may
have made it difficult to assess the difference in risk between
exclusive breastfeeding and predominant breastfeeding.
Implications
Our findings have two important implications for child health
programmes and policies. First, the extremely high risks of mor
-
tality and morbidity associated with infants who are not breast
-
fed compared with those who are predominantly or exclusively
breastfed need to be taken into account when informing HIV-
infected mothers of the risks and benefits of breastfeeding. The
high risk of infant mortality associated with partial breastfeed
-
ing (compared with predominant or exclusive breastfeeding)
coupled with an earlier report of an increased risk of HIV trans-
mission among children who are partially breastfed (compared
with those who are exclusively breastfed) (3, 4) reinforces the
need to discourage partial breastfeeding by both HIV-infected
mothers and uninfected mothers.
Second, our finding that the risks of death are similar
among infants who have been predominantly breastfed and
those who have been exclusively breastfed implies that promo-
tion programmes aimed at encouraging exclusive breastfeed-
ing would have little impact on child survival in settings where
rates of predominant breastfeeding are already high, such as in
rural Ghana. However, a large impact could be achieved in areas
where partial breastfeeding and not breastfeeding are common,
such as in urban India and Peru. The potential impact of pro-
grammes to promote exclusive breastfeeding on child survival
therefore needs to be refined, taking into account the prevalence
of exclusive breastfeeding plus predominant breastfeeding as
well as the prevalence of partial breastfeeding. The common
practice has been to calculate impact estimates by applying the
risks associated with non-breastfeeding to the prevalence of
non-exclusive breastfeeding (8). O
Acknowledgements
The support provided by the Indian Council of Medical
Research in India and by the Ministries of Health and local
health authorities in Ghana and Peru is acknowledged.
We also acknowledge the support of the WHO/CHD
Immunization-Linked Vitamin A Group. Members are listed
below.
Ghana: P. Arthur (Kintampo Health Research Centre,
Ghana, and London School of Hygiene and Tropical Medicine);
B.R. Kirkwood, S. Morris (London School of Hygiene and
Tropical Medicine); S. Amenga-Etego, C. Zandoh, and O.
Boahen (Kintampo Health Research Centre).
424
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Infant feeding patterns and risks of death Rajiv Bahl et al.
Table 5. Effect of feeding pattern on risk of all-cause hospitalization, diarrhoea-specific hospitalization and acute lower
respiratory infection-specific hospitalization among infants aged 6–26 weeks in Ghana, India and Peru. All analyses adjusted for
by site, period of follow-up and their interactions
All-cause hospitalization Diarrhoea-specific hospitalization ALRI-specific hospitalization
a
Feeding Infant- No. of Unadjusted Adjusted No. of Unadjusted Adjusted No. of Unadjusted Adjusted
pattern years of events rate ratio
b
rate ratio
c
events rate ratio rate ratio
c
events rate ratio rate ratio
c
follow-up
Exclusively 603.7 21 0.72 0.77 4 0.61 0.67 12 0.81 0.86
breastfed
d
(0.44–1.18) (0.47–1.25) (0.20–1.81) (0.23–2.01) (0.42–1.54) (0.45–1.64)
Predomi- 1587.2 109 1.0 1.0 24 1.0 1.0 47 1.0 1.0
nantly
breastfed
Partially 1011.1 66 1.15 1.12 33 1.61 1.57 31 1.02 1.03
breastfed (0.79–1.66) (0.78–1.62) (0.85–3.06) (0.83–2.96) (0.61–1.71) (0.61–1.73)
Not 61.5 13 3.77 3.39 8 6.26 5.59 5 2.75 2.50
breastfed (1.99–7.14) (1.74–6.61) (2.56–15.3) (2.17–14.4) (1.06–7.10) (0.93–6.74)
a
ALRI = acute lower respiratory infection.
b
Values in parentheses are 95% confidence intervals.
c
Adjusted for infant’s weight at enrolment, sex, twin status, birth order, and mother’s educational level, place of defecation , and household water supply.
d
A full explanation of the feeding categories can be found in the text.
India: N. Bhandari, R. Bahl, M.K. Bhan (All India Insti-
tute of Medical Sciences, New Delhi); and M.A. Wahed (Inter
-
national Center for Diarrhoeal Disease Research, Bangladesh).
Peru: M.E. Penny, C.F. Lanata, B. Butron, A.R. Huapaya,
and K.B. Rivera (Instituto de Investigación Nutricional, Lima).
Data Management: L.H. Moulton, M. Ram, C.L.
Kjolhede, and L. Propper (Johns Hopkins University, Depart
-
ment of International Health, Baltimore, MD).
Coordination: J. Martines and B. Underwood (WHO).
Funding: The Immunization-Linked Vitamin A study was
funded by the Child Health and Development Division of
WHO and the Johns Hopkins Family Health and Child
Survival Cooperative agreement (HRN 5986-A-00-6006-00),
with funding from the United States Agency for International
Development.
Competing interests: none declared.
Résumé
Alimentation du nourrisson et risques de décès et d’hospitalisation dans les six premiers mois : étude de
cohorte multicentrique
Objectif Déterminer lassociation entre différents modes
d’alimentation des nourrissons (allaitement maternel exclusif,
allaitement maternel prédominant, allaitement maternel
partiel et absence d’allaitement maternel) et la mortalité et les
hospitalisations pendant les six premiers mois.
Méthodes Le présent document s’appuie sur une analyse
secondaire des données provenant d’un essai contrôlé randomisé
multicentrique sur la supplémentation en vitamine A associée à
la vaccination. Au total, 9424 enfants et leurs mères (2919 au
Ghana, 4000 en Inde et 2505 au Pérou) ont été inclus dans l’essai
alors que les nourrissons avaient entre 18 et 42 jours dans deux
taudis urbains de New Delhi (Inde), un bidonville périurbain de
Lima (Pérou) et 37 villages du district de Kintampo (Ghana). Des
visites au domicile des couples mère-enfant ont été effectuées à
des intervalles de 4 semaines à compter de l’administration au
nourrisson de la première dose de vaccin antipoliomyélitique b
uccal et de vaccin antidiphtérique-anticoquelucheux-antitétanique,
à 6 semaines au Ghana et en Inde et à 10 semaines au Pérou.
A chaque visite, les mères devaient dire ce qu’elles avaient
proposé à boire ou à manger à leur nourrisson au cours de la
semaine écoulée. Des données ont aussi été recueillies sur les
hospitalisations et les décès de nourrissons entre 6 semaines
et 6 mois. Les principaux critères de jugement utilisés étaient la
mortalité toutes causes confondues, la mortalité par diarrhée,
la mortalité due à des infections aiguës des voies respiratoires
inférieures et les hospitalisations.
Résultats Le risque de décès ne variait pas sensiblement selon
que les enfants étaient nourris au sein exclusivement ou de façon
prédominante (rapport des risques ajustés (RR) = 1,46 ; intervalle
de confiance à 95% (IC) = 0,75-2,86). Le risque de décès était
plus élevé pour les enfants n’étant pas nourris au sein que pour
les enfants nourris au sein de façon prédominante (RR = 10,5 ;
IC à 95% = 5,0-22,0 ;
p
< 0,001), ce qui était également le cas
des enfants nourris partiellement au sein (RR = 2,46 ; IC à 95% =
1,44-4,18 ;
p
= 0,001).
Conclusion Ces résultats ont deux incidences majeures.
Premièrement, le risque de mortalité infantile extrêmement élevé
associé à l’absence d’allaitement au sein doit être pris en compte
dans les options propoes aux res infectées par le VIH concernant
l’alimentation de leur nourrisson. Deuxièmement, compte tenu
des risques de décès similaires pour les nourrissons nourris au
sein de façon prédominante et pour ceux qui sont nourris au sein
exclusivement, les mesures de promotion, les taux d’allaitement
au sein prédominant sont déjà élevés, devraient viser à maintenir
ces taux élevés et non à tenter de substituer l’alimentation au sein
exclusive à l’alimentation au sein prédominante.
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Bulletin of the World Health Organization
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Rajiv Bahl et al. Infant feeding patterns and risks of death
Resumen
Pautas de alimentación del lactante y riesgos de defunción y hospitalización en la primera mitad de la
lactancia: estudio multicéntrico de cohortes
Objetivo Determinar la relación existente entre diferentes
pautas de alimentación de los lactantes (lactancia materna
como alimentación exclusiva, predominante, parcial o nula) y la
mortalidad y los ingresos hospitalarios durante la primera mitad
de la lactancia.
Métodos Este artículo se basa en un análisis secundario de
los datos aportados por un ensayo controlado aleatorizado
multicéntrico sobre la administración de suplementos de vitamina
A vinculada a la inmunización. En total, 9424 pares de madre y
lactante (2919 en Ghana, 4000 en la India y 2505 en el Perú)
entraron a participar en este estudio cuando los lactantes tenían
18–42 días en dos barrios pobres urbanos de Nueva Delhi, India,
un poblado periurbano de chabolas de Lima, Perú, y 37 aldeas
del distrito de Kintampo en Ghana. Cada madre y lactante
fueron visitados en su vivienda a intervalos de 4 semanas desde
el momento en que el niño recibió la primera dosis de vacuna
antipoliomielítica oral y de difteria-tétanos-tos ferina, a la edad
de 6 semanas en Ghana y la India, y de 10 semanas en el Perú.
En cada visita se preguntaba a las madres qué habían dado de
comer y beber al niño durante la última semana. También se recogía
información sobre los ingresos hospitalarios y las defunciones
que se hubieran producido entre las 6 semanas y los 6 meses. Las
principales medidas de resultado fueron la mortalidad por todas
las causas, la mortalidad específica por diarrea, la mortalidad
por infecciones agudas de las vías respiratorias inferiores y los
ingresos en hospitales.
Resultados No se observó ninguna diferencia importante entre el
riesgo de defunción de los niños que fueron amamantados como
alimentación exclusiva y los alimentados predominantemente al
pecho (razón de riesgo (RR) ajustada = 1,46; intervalo de confianza
(IC) del 95% = 0,75–2,86). Los lactantes no amamantados
presentaron un mayor riesgo de morir que los predominantemente
amamantados (RR = 10,5; IC95% = 5,0–22,0; P < 0,001), y lo
mismo ocurrió con los alimentados al pecho de forma parcial
(RR = 2,46; IC95% = 1,44–4,18; P = 0,001).
Conclusión Estos resultados tienen dos implicaciones muy
importantes. Primero, a la hora de informar a las madres infectadas
por el VIH acerca de las opciones para alimentar a sus lactantes,
hay que tener en cuenta el riesgo extremadamente alto de
mortalidad infantil asociado a la ausencia de lactancia natural.
Segundo, nuestro hallazgo de un riesgo de defunción semejante
para los lactantes que sólo recibieron leche materna y los que se
alimentaron predominantemente de ese modo lleva a pensar que,
en los entornos donde las tasas de lactancia natural predominante
son ya elevadas, las actividades de promoción deben centrarse
en mantener esas tasas altas, antes que en intentar forzar un
cambio de lactancia materna predominante a lactancia materna
exclusiva.
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Infant feeding patterns and risks of death Rajiv Bahl et al.
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    • "This is in accordance with the numerous previous studies emphasising the protective effects of breastfeeding against infections [49][50][51][52]. For example, exclusive breastfeeding in the first 4-6 months postpartum has been associated with a reduction of upper and lower respiratory infections in infants [53,54]. Further, bioactive components of breastmilk were found to protect against pneumonia, mainly caused by viral infections, during infancy [55,56]. "
    [Show abstract] [Hide abstract] ABSTRACT: Human milk (HM) is a complex biofluid conferring nutritional, protective and developmental components for optimal infant growth. Amongst these are maternal cells, which change in response to feeding and were recently shown to be a rich source of miRNAs. We used next generation sequencing to characterize the cellular miRNA profile of HM collected before and after feeding. HM cells conserved higher miRNA content than the lipid and skim HM fractions or other body fluids, in accordance with previous studies. In total, 1467 known mature and 1996 novel miRNAs were identified, with 89 high-confidence novel miRNAs. HM cell content was higher post-feeding (p < 0.05), and was positively associated with total miRNA content (p = 0.014) and species number (p < 0.001). This coincided with upregulation of 29 known and 2 novel miRNAs, and downregulation of 4 known and 1 novel miRNAs post-feeding, but no statistically significant change in expression was found for the remaining miRNAs. These findings suggest that feeding may influence the miRNA content of HM cells. The most highly and differentially expressed miRNAs were key regulators of milk components, with potential diagnostic value in lactation performance. They are also involved in the control of body fluid balance, thirst, appetite, immune response, and development, implicating their functional significance for the infant.
    Full-text · Article · Jun 2016
    • "The intestinal colonisation of the neonate starts immediately after birth and is essential for the maturation of the lymphoid tissue associated to the intestine. During breastfeeding this is the only moment at which the human being not only receives all the necessary nutrients in one single food, but also this food meets the requirements suited to the functional immaturity of the digestive, kidney and immune systems of the baby (Bahl et al., 2005). In the healthy child, the introduction of artificial formulae for feeding and of supplementary foodstuffs at later stages is one of the first immunological and nutritional challenges faced by the infant and small child. "
    Full-text · Dataset · May 2016 · International Journal of Molecular Sciences
    • "Its effect is multidimensional, which may include fatigue, practicality etc. Thus the current study aimed at understanding the perceptions of the mothers in rural areas of Amroha district of Uttar Pradesh about the importance of breast feeding and the actual practices followed by them and further to study the various factors which play a role in it [25][26][27][28][29][30]. For the process of data collection, semi–structured interview schedule made in English which was converted into Hindi was used in order to collect the data from the respondents. "
    Article · Jan 2016 · International Journal of Molecular Sciences
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