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Am J Clin Nutr 2013;98:983–93. Printed in USA. Ó 2013 American Society for Nutrition 983
Nevertheless, in most populations, meat is not introduced early NGG received individual nutrition counseling with face-to-face
and is generally used in small amounts. sessions and detailed verbal and written guidance from re-
Our unpublished research with infants living in poor socio- searchers (see supplemental material under “Supplemental data”
economic conditions in Bogota, Colombia (a group at known risk in the online issue for examples). Guidelines focused on the
of stunting and iron deficiency), identified several undesirable following 3 main messages that were emphasized at all study
practices during the CF period, including the early introduction of visits: 1) the importance of continuing breastfeeding alongside
infant formula and low intakes of iron and vitamin A. On the basis CF; 2) the importance of including red meat as a source of iron
of these data, we developed new CF guidelines to meet the es- to prevent anemia; and 3) the importance of fruit and vegetables
timated nutritional requirements of infants aged 6–12 mo of age as part of a healthy diet. Mothers were offered specific advice
(WHO), with a focus on the use of red meat, including cheaper on the number of portions of meat that should be given ($5
and widely available iron-rich meats such as chicken liver, to portions/wk, including red meat $3 times/wk); mothers were
improve iron and zinc status. In this randomized controlled trial, also advised to include chicken liver and heart as affordable
we tested the efficacy and safety of the new CF guidelines in the forms of meat, and suggestions were given for the preparation of
same population. Our specific hypothesis was that the new recommended foods. Mothers were also advised to give fruit and
guidelines would result in 1) increased red meat intake, 2) im- vegetables daily. Menu plans were provided at each study visit,
proved iron and zinc status, and 3) improved linear growth, including suggestions for the number of meals, types of com-
without adverse effects on adiposity or breastfeeding. We also plementary foods, suggested amounts to be offered, recipes, and
investigated the acceptability and affordability of the new guide- advice on food hygiene. Mothers also received a leaflet with
lines and tolerance of the complementary foods recommended. additional general recommendations and tips to improve their
knowledge and confidence in feeding their babies (see online
supplementary materials 1 and 2 under “Supplemental data” in
SUBJECTS AND METHODS the online issue).
Mothers randomly assigned to the CG received the standard
Subjects
advice on CF from health care professionals in the growth-
Mothers of healthy term infants with birth weight .2500 g monitoring program. This information included advice on
who were participating in the growth-monitoring program at 2 breastfeeding, general recommendations on suitable comple-
hospitals in Bogota, Colombia (Fontibon and Suba), and who mentary foods including meat, food hygiene, and food prepa-
were exclusively breastfeeding when their infants were 4 mo of ration; however, no specific advice was given on the frequency or
age were approached and given information about the study. amount of foods that should be offered.
Both hospitals serve populations with low socioeconomic status; Where possible, visits were scheduled at the same time as
family incomes come mainly from informal and part-time jobs, those that were part of the growth-monitoring scheme. Mothers
most families live in rented or shared households, and w29% of were reimbursed for their travel expenses. All participants re-
the population experience food insecurity (31), although 97% of ceived a weaning set consisting of a bowl and spoon as a gift for
the population has public services coverage including tap water, participating, and these sets were also used to standardize the
electricity, and waste disposal. Parasitic infections are uncommon assessment of food portions. At the end of the study, the mother
in infants in this population, and malaria does not occur in Bogota. also received an infant-feeding beaker.
Mothers who were willing to participate and who were still
breastfeeding when their infants were 6 mo of age gave written
informed consent. A baseline hemoglobin measurement was Outcome measures were recorded as follows
performed; infants with a hemoglobin concentration ,11 g/dL
1) Anthropometric measures were performed at each visit.
(the cutoff used to define anemia in Colombia) were excluded
Length was measured by using an infantometer with
from additional participation in the study and were referred to
a fixed headboard and movable footboard to the nearest
a physician for treatment. Eligible subjects were randomly as-
1 mm. The mean of 3 measurements was used. Infants
signed to either the new guidelines group (NGG) or control
were weighed naked on an electronic scale (Tanita). Head
group (CG). Random assignment was stratified by hospital and
circumference and midupper arm circumference were
whether or not CF had been introduced to infants between 4 and
measured to the nearest 1 mm by using a nonstretchable
6 mo of age. Randomization assignments were prepared by
measuring tape. Results were converted to SD scores by
using randomized blocks of permuted length by a member of the
using WHO 2007 growth-standard data (32).
team who had no contact with study subjects and were stored in
sealed opaque envelopes. It was not possible to blind researchers 2) A blood sample was obtained at 6 and 12 mo of age to
who collected anthropometric and food-intake data, but labo- measure hemoglobin, hematocrit, serum ferritin (SF), and
ratory measurements were blinded. The study was approved by zinc. Hemoglobin was measured by using spectropho-
the research ethics committees at University College London tometry; mean corpuscular volume (MCV) and hemato-
and Pontificia Universidad Javariana. This trial was registered at crit were measured by using automated flow cytometry.
http://isrctn.org as ISRCTN57733004. SF was measured by using a 2-site ELISA (DALTIS-
Dizar). Assays were calibrated from 0 to 1000 ng/mL
by using Quimiolab controls (Colombian external quality-
Treatment of subjects control program). Sensitivity was 1.0 ng/mL, and specific-
Subjects were seen at clinic visits when infants were 6, 8, 10, ity was measured by using controls from human liver
and 12 mo of age. Infants who were randomly assigned to the ferritin, spleen ferritin, and cardiac ferritin from Quimiolab
FIGURE 1. Flowchart of subject progress through the study. CONSORT, Consolidated Standards of Reporting Trials.
controls. Serum zinc samples were collected in the morning fruit, and vegetables) was recorded at 6, 8, 10, and 12 mo
(nonfasting) by following the protocol recommended by of age by using a semiquantitative food-frequency ques-
the International Zinc Nutrition Consultative Group in their tionnaire. The frequency and number of portions of each
technical document (33); samples were processed by using food consumed on each occasion were recorded; fre-
zinc-free needles, syringes, centrifuge tubes, storage vials, quency was defined as follows: daily denoted food con-
and transfer pipettes, with avoidance of hemolysis and con- sumed on all 7 d of the week, weekly denoted foods
tamination. Blood was stored in the refrigerator and centri- consumed $4 d/wk (excluding foods that were consumed
fuged to separate the serum, which was frozen before daily), and monthly denoted food consumed $2/mo.
analysis by using atomic absorption spectrophotometry. Breast-milk consumption was assessed by taking into
C-reactive protein (CRP) was measured by using a 2-site account 1) the number of breastfeeds per day, 2) the time
ELISA (ADALTIS-Dizar) and used as a biomarker of in- required for each breastfeed, and 3) the number of breast-
flammation with CRP concentrations .6 mg/L considered feeds per night.
abnormal.
4) The acceptability, tolerance and affordability of recom-
For the analysis of iron and zinc status the following cutoffs mendations in the NGG were assessed by using a ques-
recommended by the WHO were used: hemoglobin concen- tionnaire completed by mothers when infants were 8, 10,
tration ,11 g/dL, hematocrit ,33%, and SF concentration and 12 mo of age. Acceptability was assessed by using
,12 mg/L (34); MCV ,70 fL (35); and serum zinc concen-
a scale from 1 to 3 [1 = disliked (baby did not accept
tration ,65 mg/dL (34–36).
food), 2 = liked (baby accepted the food), and 3 = liked
3) The intake of foods specifically highlighted by the new very much (baby accepted and enjoyed the food)]. Com-
guidelines (meat, red meat, milk other than breast milk, plementary food tolerance was defined as tolerated and
not tolerated [1 = tolerated (baby took and ate the com- groups by using the t test for continuous variables (hemoglobin,
plementary food) and 2 = not tolerated (baby did not eat hematocrit, MCV, zinc, and anthropometric variables) and the
the CF or ate it but it caused distress, vomiting, or other chi-square test for categorical variables (cutoffs for hemoglobin,
symptoms)]. Affordability was assessed by using a scale SF, zinc, and food-consumption variables). SF concentrations at
of 1 or 2 (1 = affordable (if the mother had been able to 6 and 12 mo of age were not normally distributed and were log
buy the CFs recommended $3 times/wk, and 2 = not transformed for analysis. For anthropometric variables and
affordable (if the mother could not buy some of the markers of iron and zinc status, we compared the values at 12 mo
CFs recommended)]. of age and the change from 6 to 12 mo of age between randomly
assigned groups. ANCOVA was also performed to examine
differences in the change in anthropometric or biochemical
Statistics variables from 6 to 12 mo of age between randomly assigned
Sample size groups with adjustment for baseline values and, where appro-
The sample size of 64 infants/group was calculated to detect priate, potential confounders and to test for interactions between
a 0.5-SD difference in outcome measures at a = 0.05 with 80% baseline values and randomly assigned groups on outcomes.
power, which we considered to be biologically relevant and
plausible given our previous studies that used nutritional in-
RESULTS
terventions in infants. The sample size was considered to be
achievable within the timeframe for the study given local figures Effect of the randomized intervention
on infant-feeding practices, notably reported rates of exclusive
The planned sample size could not be achieved within the
breastfeeding at 4 mo of age (37). To allow for losses to follow-
timeframe of the study, mainly because the prevalence of ex-
up, we planned to randomly assign 90 infants/group.
clusive breastfeeding in Bogota had fallen, which reduced the
number of eligible infants. A total of 353 mothers who were
Data analyses exclusively breastfeeding when their infants were 4 mo of age
Data were analyzed with SPSS software (version 18; IBM). were approached (Figure 1); 168 mothers were eligible for the
Main outcomes were compared between randomly assigned study, and 116 mothers were willing to participate. A total of
TABLE 2
Comparison of breastfeeding practices at 12 mo of age between the NGG and CG by using data from a 24-h recall1
Variable NGG (n = 38) CG (n = 38) Difference2
consumed per week was also significantly higher in the NGG, higher in the NGG than CG at 12 mo of age. These differences
whereas infants in the CG consumed significantly more portions remained after adjustment for confounding factors such as sex,
per week of sweetened foods (defined as sugar, jelly, chocolate, birth weight ,3 or $3 kg, weight gain from 0 to 6 mo of age, and
and sweets), milk, and cow milk (Figure 2). Significantly more weight at 6 mo of age. SF at 12 mo of age was not significantly
infants in the NGG consumed recommended food portions per different between groups, and this finding was unchanged when 5
week at 12 mo of age, whereas infants in the CG had signifi- infants (2 infants in the NGG and 3 infants in the CG) with CRP
cantly more bottle-feeds than those of infants in the NGG, .6 were excluded from the analysis.
consumed cow milk more than 1 time/wk, and had ,2 main Changes in hemoglobin and hematocrit from 6 to 12 mo of age
meals/d There was no significant difference between groups in were positive and were significantly higher in the NGG than CG
the number of breastfeeds per day, time per breastfeed, and [mean 6 SD change in hemoglobin 0.41 6 0.8 g/dL compared
number of breastfeeds per night. with 20.13 6 1.0 (P = 0.01) and hematocrit 1.04 6 2.2%
compared with 20.15 6 2.4) (P = 0.03)]. After adjustment for
Linear growth socioeconomic factors, the change in hemoglobin from 6 to 12
The length-for-age z score (LAZ) at 6 and 12 mo of age and mo of age was negatively predicted by the hemoglobin at 6 mo
the change in LAZ were not significantly different between of age (coefficient: 20.58; 95% CI: 20.82, 20.33; P # 0.001),
groups (Table 4). The number and proportion of infants with and there was a positive effect of the randomly assigned group
a LAZ less than 22 SDs was significantly higher at 6 mo of age (coefficient: 0.56; 95% CI: 0.19, 0.92; P = 0.003). There was no
in the NGG [10 infants (23.8%)] than in the CG [2 infants interaction between hemoglobin at 6 mo of age and the ran-
(4.7%)] (P = 0.02). At 12 mo of age, there was no significant domly assigned group on the change of hemoglobin from 6 to 12
difference between groups, but the number and proportion of mo of age (P = 0.42). The change in hematocrit from 6 to 12 mo
infants with a LAZ less than 22 SDs in the CG increased from 2 of age was not related to baseline hematocrit after adjustment for
infants (4.7%) at 6 mo of age to 8 infants (21.1%) at 12 mo of socioeconomic factors, and there was no interaction between
age, whereas the number and proportion in the NGG remained hematocrit at 6 mo of age and the randomly assigned group on
similar at 12 mo of age to those at 6 mo of age. After adjustment the change in hematocrit from 6 to 12 mo of age (P = 0.73).
for baseline LAZ and socioeconomic factors, the change in LAZ SF decreased from 6 to 12 mo of age in both groups with no
from 6 to 12 mo of age was not predicted by the randomly as- significant difference between groups (227.23 6 44.8 mg/L in
signed group, and there was no interaction between the LAZ at 6 the CG compared with 213.62 6 37.3 mg/L in the NGG; 95%
mo of age and the randomly assigned group on the change in CI for difference in decline: 20.63, 33.5; P = 0.2). After ad-
LAZ from 6 to 12 mo of age (P = 0.9). justment for socioeconomic factors, baseline SF was not asso-
ciated with the change in SF from 6 to 12 mo of age, and there
Iron status was no interaction between SF at 6 mo of age and the randomly
Values of hemoglobin, hematocrit, MCV, and SF at 6 and 12 assigned group on the change in SF from 6 to 12 mo of age (P =
mo of age and the change between 6 and 12 mo of age for the 0.64).
NGG and CG are shown in Table 5. At 6 mo of age, there was no The proportion of infants who had a hemoglobin concentration
significant difference in these indicators between groups. Hemo- ,11 g/dL and hematocrit ,33% at 12 mo of age was 4 infants
globin (P = 0.009) and hematocrit (P = 0.02) were significantly (11%) in the CG and 0 infants (0%) in the NGG (P = 0.1). The
Difference2
than in the CG (0 infants; P = 0.03) and increased at 12 mo of
age to 29% in the NGG and 37.1% in the CG (P = 0.9)
Zinc status
Serum zinc increased from 6 to 12 mo of age in both groups.
0.44
0.67
0.66
0.71
The mean increase was higher in the CG than in the NGG, but
0.3
CG (n = 38)
z score; LAZ, length-for-age z score; MUACZ, midupper arm circumference z score; NGG, new guidelines group; WAZ, weight-for-age z score; WLZ, weight-for-length z score.
there was no significant difference between groups [mean 6 SD
Change from 6 to 12 mo
6
6
6
6
6
change: 31.01 6 25.7 mg/dL in the CG compared with 20.33 6
20.006
20.19
20.27
20.26
0.28
37.3 mg/dL in the NGG (Table 5)]. The proportion of infants
with low zinc status by using a cutoff of ,65 mg/dL decreased
between 6 and 12 mo of age in both groups [36 7.7% in the
NGG (n = 38)
0.45
0.60
0.76
0.52
0.70
of age; NS].
Comparison of anthropometric measurements at 6 and 12 mo of age and the change from 6 to 12 mo of age between randomly assigned groups1
0.00)a
0.39)
0.28)
NGG infants, and similar results were observed for the WLZ and
Difference2
(20.96,
(20.84,
(20.59,
(20.57,
–0.54
20.42
20.98
20.15
0.9
1.1
0.9
0.9
0.18
0.55
20.043
The same positive correlation for this period was observed with
1–0
CG (n = 38)
0.9
1.0
0.9
0.84
0.80
0.93
1.1
0.8
2
3
HCZ
LAZ
(227.0, 5.7)
Student’s t- test: aP , 0.05, bP , 0.001. CG, control group; MCV, mean corpuscular volume; NGG, new
(20.42, 3.0)
(26.3, 33.5)
(0.11, 0.9)b
(0.12, 2.3)a
meat consumption per week and serum zinc at 12 mo of age or the
Difference2
change in serum zinc between 6 and 12 mo of age. However,
infants with red meat consumption ,3 times/wk from 6 to 8 and
210.7
0.5
13.6
1.2
1.3
10 to 12 mo of age had significantly greater increase in zinc
between 6 and 12 mo of age.
44.8
25.7
1.0
2.4
3.9
DISCUSSION
6
6
6
6
6
CG
20.13
20.15
20.20
227.2
31.0
Change from 6 to 12 mo
6
6
6
6
6
Difference2
24.23
0.97
6.31
6
6
6
6
6
11.9
35.5
71.4
114.9
17.3
a,b
age. We could not directly compare our findings with those from
3.65 (28.8, 16.0)
40.5
19.3
controlled trials (RCTs) (28, 29, 40) that investigated meat or red
43.4
88.7
6 mo of age
30.3
29.7
0.73
1.9
3.8
Ferritin (mg/L)
Variable
Zinc (mg/dL)
2
3
a higher meat intake during the first year was associated with
a higher hemoglobin concentration. Some cluster randomized
trials that used nutrition education combined with recommen- in the CG, suggested a possible protective effect of the in-
dations to improve CF (21–27) have reported significantly in- tervention. Our findings were in agreement with those from 3
creased meat consumption but did not focus on the effect of RCTs that investigated meat as a CF food, albeit by using dif-
meat consumption on iron and zinc status. ferent indicators (28, 29, 40), and with those from a cluster
Other strategies such as iron supplementation and sprinkles randomized study in Pelotas, Brazil (26). Conversely, studies in
have been used to improve iron status in infants with conflicting Pakistan (25), China (23), and Peru (22) reported positive effects
results, and RCTs that used sprinkles were generally testing the of interventions on growth.
treatment rather than primary prevention (20, 42). In a blinded Although the approach used to deliver the messages recom-
RCT in Honduras and Sweden, iron supplementation from 4 to 9 mended in the new CF guidelines was feasible and successful in
mo of age resulted in a significant increase in hemoglobin and the setting of this study, the implications in terms of staffing and
reduced iron deficiency anemia in Honduras but not in Sweden resources need to be evaluated before the guidelines can be more
(16), where impaired linear growth was observed (17). A study in widely used. The messages were delivered by researchers, and
Indian infants also reported a negative effect of iron supple- each session lasted w45 min, which was longer than the time
mentation on growth (43). In addition, compliance with iron currently allocated for routine clinic visits. It would also be
supplementation is often very low (15, 44). important to examine in more detail which parts of the guide-
We showed no significant effect of the intervention on zinc lines and their delivery were most important for success because
status at 12 mo of age or a change in zinc status from 6 to 12 mo of this might allow them to be implemented in a more-efficient
age. Serum zinc concentrations increased in both groups and way. This issue was not examined in this study, but several of the
were not correlated with the frequency of red meat consumption following possible factors may have contributed to the effective
per week, which were results similar those in a randomized trial uptake of the guidelines: 1) the guidelines were designed on the
of meat compared with micronutrient fortified cereals in US basis of local culture, food availability, environment, and infant
infants (28). However, we showed that those infants who ate red characteristics; 2) individual counseling sessions allowed edu-
meat ,3 times/wk had greater and more-positive changes in cational messages to be adapted to individual needs and un-
zinc status compared with those who ate red meat more fre- derstandings; 3) the 3 main messages were repeated and reinforced
quently, which suggested potential negative effects of increased by written materials; and 4) emphasis was given to the importance
red meat consumption on zinc status. It is plausible that iron in of the recommendations for the infant’s health. Our observation
red meat could interfere with zinc absorption. However, there is that grandmothers played an important role in the feeding de-
a need for additional research in this area to examine in- cisions of mother suggested that it might be worth including this
teractions between iron and zinc intakes during CF. group in any future intervention.
The intervention had no significant effect on anthropometric The main strength of the study was the randomized design,
measures at 12 mo of age or on changes in z scores between 6 and which allowed for causal relations between the intervention and
12 mo of age. A greater proportion of infants in the NGG had outcomes to be established. Compliance with the protocol was
linear stunting at 6 mo of age, but because this proportion did good, and there was low attrition. The main limitation of the study
not increase by 12 mo of age in the NGG, whereas it increased was the relatively small sample size, which limited the power for
some analyses. With 38 subjects per group, we had 80% power to analyses, manuscript writing, and critical reading of the manuscript; and
detect a difference of a 0.69 SD at 5% significance and could have ML and MSF: design of new CF guidelines and trial, data interpretation,
missed a smaller, although perhaps clinically relevant, effect on and critical reading and revision of manuscript. None of the authors declared
a conflict of interest following the guidelines of the International Committee
outcomes. The small sample size also resulted in a baseline
of Medical Journal Editors.
imbalance in anthropometric measures between groups, which
we addressed by comparing differences in outcome variables
adjusted for the baseline value and testing for interactions be- REFERENCES
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