Efficacy and safety of new complementary feeding guidelines with an emphasis on red meat consumption: a randomized trial in Bogota, Colombia1–3 ABSTRACT Background: Iron deficiency and poor linear growth are common in infants from deprived socioeconomic backgrounds and may be associated with inadequate complementary feeding (CF) practices. Objective: We tested the hypothesis that new CF guidelines emphasizing meat as a source of iron and zinc would improve linear growth, iron, and zinc status in infants living in poor socioeconomic circumstances in Bogota, Colombia. Design: A total of 85 term infants who were exclusively breastfed for $4 mo were randomly assigned at 6 mo of age to a control group [CG (n = 43); current advice] or intervention group (new guidelines group [NGG (n = 42); with counseling to 1) continue breastfeeding, 2) offer red meat $3 d/wk, and 3) offer fruit and vegetables daily]). Main outcomes were 1) linear growth from 6 to 12 mo of age; 2) hemoglobin, hematocrit, iron [serum ferritin (SF)], and zinc status at 12 mo of age; and 3) meat intake at 12 mo of age (by using a food-frequency questionnaire). Results: A total of 38 infants/group provided data at 12 mo of age. NGG infants had significantly higher red meat intake [mean 6 SD: 5.4 6 1.8 compared with 3.5 6 1.7 d/wk at 12 mo of age; P , 0.001), higher hemoglobin and hematocrit at 12 mo of age, and a significantly greater increase in hemoglobin (mean 6 SD change: 0.41 6 0.8 compared 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) from 6 to 12 mo of age than those in CG infants. There were no significant differences in linear growth from 6 to 12 mo of age or in SF or zinc. Conclusions: The new guidelines showed efficacy with higher red meat intake and positive effects on hemoglobin and hematocrit. The intervention was acceptable and affordable for most mothers. These preliminary results suggest that the intervention merits investigation in a larger cohort with longer-term follow-up. This trial was registered at http://isrctn.org as ISRCTN57733004. Am J Clin Nutr 2013;98:983–93. INTRODUCTION

Complementary foods are introduced into the infant diet to complement breast milk at a stage when sufficient amounts of certain nutrients, notably iron and zinc, can no longer be provided by breast milk alone. The WHO recommends that complementary feeding (CF)4 should start from 6 mo of age (1, 2). However, despite much discussion about the timing of the introduction of CF, there has been little research on whether the type of complementary foods introduced influences infant growth, nutritional status, and health outcomes.

Iron deficiency is common during the CF period, particularly in vulnerable populations with a high prevalence of maternal iron deficiency, low birth weight, infection, and poor dietary intakes and may be associated with adverse effects on cognitive outcome (3, 4). Zinc deficiency is also common and is associated with poor linear growth and increased infection risk (5–9). Both micronutrients are present in low concentrations in breast milk, albeit with high bioavailability, and it is recognized that infants who are exclusively breastfed for w6 mo require a good source of these nutrients during CF, either directly from foods or as supplements (10–12). Strategies for improving micronutrient intake in low-income populations include food fortification, sprinkles, and micronutrient supplements (13–20). Interventions that used educational strategies to improve CF have shown positive effects on meat consumption but have not focused on the effect on iron and zinc status (21–27). Meat is a good source of bioavailable zinc and iron as well as protein. In a randomized trial in the United States, meat was acceptable to mothers and infants as an early CF and associated with a trend toward better behavioral outcomes at 12 mo of age (28), whereas Danish infants randomly assigned to receive a higher meat intake had a smaller decrease in hemoglobin in late infancy (29). A cohort study in the United Kingdom reported positive associations between meat intake from 4 to 12 mo of age and weight gain at #12 mo of age and psychomotor development at 22 mo of age (30).

1

From the Nutrition and Biochemistry Department, Faculty of Sciences, Pontificia Universidad Javeriana, Bogota, Colombia (GAO), and the Childhood Nutrition Research Centre, University College London Institute of Child Health, London, United Kingdom (GAO, MSF, and ML). 2 Supported by the Childhood Nutrition Research Centre, University College London Institute of Child Health, and Pontificia Universidad Javeriana. Tommee Tippee (United Kingdom) donated the feeding spoons, cups, and beakers used in the study. 3 Address correspondence to MS Fewtrell, Childhood Nutrition Research Centre, University College London Institute of Child Health, 30 Guilford Street, London WC1N 1EH. E-mail: [email protected] 4 Abbreviations used: CF, complementary feeding; CG, control group; CRP, C-reactive protein; LAZ, length-for-age z score; MCV, mean corpuscular volume; MUAC, midupper arm circumference; MUACZ, midupper arm circumference z score; NGG, new guidelines group; RCT, randomized controlled trial; SF, serum ferritin; WAZ, weight-for-age z score; WLZ, weight-for-length z score. Received January 25, 2013. Accepted for publication July 9, 2013. First published online August 14, 2013; doi: 10.3945/ajcn.112.053595.

Am J Clin Nutr 2013;98:983–93. Printed in USA. Ó 2013 American Society for Nutrition

983 Supplemental Material can be found at: http://ajcn.nutrition.org/content/suppl/2013/09/16/ajcn.112.0 53595.DCSupplemental.html

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Gilma A Olaya, Margaret Lawson, and Mary S Fewtrell

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OLAYA ET AL

SUBJECTS AND METHODS

Subjects Mothers of healthy term infants with birth weight .2500 g who were participating in the growth-monitoring program at 2 hospitals in Bogota, Colombia (Fontibon and Suba), and who were exclusively breastfeeding when their infants were 4 mo of age were approached and given information about the study. Both hospitals serve populations with low socioeconomic status; family incomes come mainly from informal and part-time jobs, most families live in rented or shared households, and w29% of the population experience food insecurity (31), although 97% of the population has public services coverage including tap water, electricity, and waste disposal. Parasitic infections are uncommon in infants in this population, and malaria does not occur in Bogota. 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 performed; infants with a hemoglobin concentration ,11 g/dL (the cutoff used to define anemia in Colombia) were excluded from additional participation in the study and were referred to a physician for treatment. Eligible subjects were randomly assigned to either the new guidelines group (NGG) or control group (CG). Random assignment was stratified by hospital and whether or not CF had been introduced to infants between 4 and 6 mo of age. Randomization assignments were prepared by using randomized blocks of permuted length by a member of the team who had no contact with study subjects and were stored in sealed opaque envelopes. It was not possible to blind researchers who collected anthropometric and food-intake data, but laboratory measurements were blinded. The study was approved by the research ethics committees at University College London and Pontificia Universidad Javariana. This trial was registered at http://isrctn.org as ISRCTN57733004. Treatment of subjects Subjects were seen at clinic visits when infants were 6, 8, 10, and 12 mo of age. Infants who were randomly assigned to the

NGG received individual nutrition counseling with face-to-face sessions and detailed verbal and written guidance from researchers (see supplemental material under “Supplemental data” in the online issue for examples). Guidelines focused on the following 3 main messages that were emphasized at all study visits: 1) the importance of continuing breastfeeding alongside CF; 2) the importance of including red meat as a source of iron to prevent anemia; and 3) the importance of fruit and vegetables as part of a healthy diet. Mothers were offered specific advice on the number of portions of meat that should be given ($5 portions/wk, including red meat $3 times/wk); mothers were also advised to include chicken liver and heart as affordable forms of meat, and suggestions were given for the preparation of recommended foods. Mothers were also advised to give fruit and vegetables daily. Menu plans were provided at each study visit, including suggestions for the number of meals, types of complementary foods, suggested amounts to be offered, recipes, and advice on food hygiene. Mothers also received a leaflet with 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 the online issue). Mothers randomly assigned to the CG received the standard advice on CF from health care professionals in the growthmonitoring program. This information included advice on breastfeeding, general recommendations on suitable complementary foods including meat, food hygiene, and food preparation; however, no specific advice was given on the frequency or amount of foods that should be offered. Where possible, visits were scheduled at the same time as those that were part of the growth-monitoring scheme. Mothers were reimbursed for their travel expenses. All participants received a weaning set consisting of a bowl and spoon as a gift for participating, and these sets were also used to standardize the assessment of food portions. At the end of the study, the mother also received an infant-feeding beaker.

Outcome measures were recorded as follows 1) Anthropometric measures were performed at each visit. Length was measured by using an infantometer with a fixed headboard and movable footboard to the nearest 1 mm. The mean of 3 measurements was used. Infants were weighed naked on an electronic scale (Tanita). Head circumference and midupper arm circumference were measured to the nearest 1 mm by using a nonstretchable measuring tape. Results were converted to SD scores by using WHO 2007 growth-standard data (32). 2) A blood sample was obtained at 6 and 12 mo of age to measure hemoglobin, hematocrit, serum ferritin (SF), and zinc. Hemoglobin was measured by using spectrophotometry; mean corpuscular volume (MCV) and hematocrit were measured by using automated flow cytometry. SF was measured by using a 2-site ELISA (DALTISDizar). Assays were calibrated from 0 to 1000 ng/mL by using Quimiolab controls (Colombian external qualitycontrol program). Sensitivity was 1.0 ng/mL, and specificity was measured by using controls from human liver ferritin, spleen ferritin, and cardiac ferritin from Quimiolab

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Nevertheless, in most populations, meat is not introduced early and is generally used in small amounts. Our unpublished research with infants living in poor socioeconomic conditions in Bogota, Colombia (a group at known risk of stunting and iron deficiency), identified several undesirable practices during the CF period, including the early introduction of infant formula and low intakes of iron and vitamin A. On the basis of these data, we developed new CF guidelines to meet the estimated nutritional requirements of infants aged 6–12 mo of age (WHO), with a focus on the use of red meat, including cheaper and widely available iron-rich meats such as chicken liver, to improve iron and zinc status. In this randomized controlled trial, we tested the efficacy and safety of the new CF guidelines in the same population. Our specific hypothesis was that the new guidelines would result in 1) increased red meat intake, 2) improved iron and zinc status, and 3) improved linear growth, without adverse effects on adiposity or breastfeeding. We also investigated the acceptability and affordability of the new guidelines and tolerance of the complementary foods recommended.

EFFICACY OF NEW COMPLEMENTARY FEEDING GUIDELINES

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controls. Serum zinc samples were collected in the morning (nonfasting) by following the protocol recommended by the International Zinc Nutrition Consultative Group in their technical document (33); samples were processed by using zinc-free needles, syringes, centrifuge tubes, storage vials, and transfer pipettes, with avoidance of hemolysis and contamination. Blood was stored in the refrigerator and centrifuged to separate the serum, which was frozen before analysis by using atomic absorption spectrophotometry. C-reactive protein (CRP) was measured by using a 2-site ELISA (ADALTIS-Dizar) and used as a biomarker of inflammation with CRP concentrations .6 mg/L considered abnormal. For the analysis of iron and zinc status the following cutoffs recommended by the WHO were used: hemoglobin concentration ,11 g/dL, hematocrit ,33%, and SF concentration ,12 mg/L (34); MCV ,70 fL (35); and serum zinc concentration ,65 mg/dL (34–36). 3) The intake of foods specifically highlighted by the new guidelines (meat, red meat, milk other than breast milk,

fruit, and vegetables) was recorded at 6, 8, 10, and 12 mo of age by using a semiquantitative food-frequency questionnaire. The frequency and number of portions of each food consumed on each occasion were recorded; frequency was defined as follows: daily denoted food consumed on all 7 d of the week, weekly denoted foods consumed $4 d/wk (excluding foods that were consumed daily), and monthly denoted food consumed $2/mo. Breast-milk consumption was assessed by taking into account 1) the number of breastfeeds per day, 2) the time required for each breastfeed, and 3) the number of breastfeeds per night. 4) The acceptability, tolerance and affordability of recommendations in the NGG were assessed by using a questionnaire completed by mothers when infants were 8, 10, and 12 mo of age. Acceptability was assessed by using a scale from 1 to 3 [1 = disliked (baby did not accept food), 2 = liked (baby accepted the food), and 3 = liked very much (baby accepted and enjoyed the food)]. Complementary food tolerance was defined as tolerated and

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FIGURE 1. Flowchart of subject progress through the study. CONSORT, Consolidated Standards of Reporting Trials.

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OLAYA ET AL TABLE 1 Baseline characteristics of mothers and infants according to randomly assigned group1 Variable

CG (n = 38)

P

24.1 6 6.4 28.8 6 9.5 1.6 6 0.70 5.3 6 1.3 2.3 6 0.9 20 (52.6)

22.9 6 5.9 25.1 6 5.6 1.5 6 0.86 5.7 6 2.3 2.7 6 1.4 25 (67.6)

0.4 0.04 0.7 0.4 0.2 0.2

19 (50) 19 (50) 39.0 (1.0)

19 (50) 19 (50) 39.2 (1.0)

1.0 — 0.5

25 (65.8) 13 (34.2)

30 (78.9) 8 (21.1)

0.3 —

3.03 6 0.28 33.9 6 1.3 20.58 6 0.6

3.1 6 0.39 33.8 6 1.3 20.34 6 0.8

0.2 0.8 0.2

2

17 (44.7) 21 (55.3) 9 (23.7) 9 (23.7) 9 (23.7) 7.25 64.9 43.0 14.3

6 6 6 6

0.73 2.38 1.14 0.91

17 21 7 6 14

(44.7) (55.3) (18.4) (15.8) (36.8)

7.86 65.6 43.4 14.9

6 6 6 6

0.99 2.05 1.34 1.15

1.0 — 0.6 0.4 0.4 0.003 0.2 0.2 0.02

1

Baseline data are shown for infants with outcome data at 12 mo of age. Mean values were compared by using Student’s t test, and categorical variables were compared by using the chi-square test. CF, complementary feeding; CG, control group; NGG, new guidelines group; MUAC, midupper arm circumference; WAZ, weight-for-age z score. 2 Mean 6 SD (all such values).

not tolerated [1 = tolerated (baby took and ate the complementary food) and 2 = not tolerated (baby did not eat the CF or ate it but it caused distress, vomiting, or other symptoms)]. Affordability was assessed by using a scale of 1 or 2 (1 = affordable (if the mother had been able to buy the CFs recommended $3 times/wk, and 2 = not affordable (if the mother could not buy some of the CFs recommended)]. Statistics Sample size The sample size of 64 infants/group was calculated to detect a 0.5-SD difference in outcome measures at a = 0.05 with 80% power, which we considered to be biologically relevant and plausible given our previous studies that used nutritional interventions in infants. The sample size was considered to be achievable within the timeframe for the study given local figures on infant-feeding practices, notably reported rates of exclusive breastfeeding at 4 mo of age (37). To allow for losses to followup, we planned to randomly assign 90 infants/group. Data analyses Data were analyzed with SPSS software (version 18; IBM). Main outcomes were compared between randomly assigned

groups by using the t test for continuous variables (hemoglobin, hematocrit, MCV, zinc, and anthropometric variables) and the chi-square test for categorical variables (cutoffs for hemoglobin, SF, zinc, and food-consumption variables). SF concentrations at 6 and 12 mo of age were not normally distributed and were log transformed for analysis. For anthropometric variables and markers of iron and zinc status, we compared the values at 12 mo 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 variables from 6 to 12 mo of age between randomly assigned groups with adjustment for baseline values and, where appropriate, potential confounders and to test for interactions between baseline values and randomly assigned groups on outcomes. RESULTS

Effect of the randomized intervention The planned sample size could not be achieved within the timeframe of the study, mainly because the prevalence of exclusive breastfeeding in Bogota had fallen, which reduced the number of eligible infants. A total of 353 mothers who were exclusively breastfeeding when their infants were 4 mo of age were approached (Figure 1); 168 mothers were eligible for the study, and 116 mothers were willing to participate. A total of

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Mother’s age (y) Father’s age (y) No. of children Family size No. of rooms in home Mother completed high school [n (%)] Sex [n (%)] F M Gestational age (wk) [n (%)] Delivery [n (%)] Vaginal Cesarean Birth Weight (kg) Head circumference (cm) WAZ Feeding practices [n (%)] CF at 4–6 mo of age CF at .6 mo of age .1 bottle-feed at 6 mo of age [n (%)] Consuming cow milk at 6 mo of age [n (%)] Eating red meat at 6 mo of age [n (%)] At 6 mo of age Weight (kg) Length (cm) Head circumference (cm) MUAC (cm)

NGG (n = 38)

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EFFICACY OF NEW COMPLEMENTARY FEEDING GUIDELINES

Compliance with, and acceptability of, the intervention

FIGURE 2. Comparison of numbers of portions per week of selected foods consumed from 10 to 12 mo of age according to the randomly assigned group. Box-and-whisker plots of numbers of portions of different foods consumed per week are shown according to the randomly assigned group. Boxes represent 25th–75th percentiles, with medians shown as lines. Bars represent highest and lowest values. Comparisons between randomly assigned groups were made by using the Mann-Whitney U test. The NGG had a significantly higher consumption of meat, red meat, fruit, and vegetables. The CG had a significantly higher consumption of milk, sugar, and sweetened foods. CG, control group; NGG, new guidelines group.

110 infants attended the screening blood test, and 22 (20%) of these infants had a hemoglobin concentration ,11 g/dL; these infants were treated with iron supplements and were not enrolled in the study. Eighty-five eligible infants were randomly assigned after the blood test, 42 infants to the NGG (20 boys) and 43 infants to the CG (21 boys). Four NGG and 5 CG infants were lost to follow-up between baseline (6 mo of age) and 12 mo of age. Baseline data for infants who also provided data at 12 mo of age are shown in Table 1 according to randomly assigned groups. For all infants randomly assigned, those in the CG were significantly heavier with higher midupper arm circumference (MUAC), weight-for-age z score (WAZ), weight-for-length z score (WLZ), and MUAC z score (MUACZ) at baseline (6 mo of age); for infants with data at 12 mo of age, CG infants were also heavier with higher MUAC at baseline. By design, similar proportions of infants from the 2 groups had started CF before 6 mo of age [19 infants (45%) in the NGG and 20 infants (51%) in

Twenty-eight mothers (74%) mothers in the NGG followed the new recommendations completely during the whole period of the intervention. Reasons given for not following the recommendations completely were family pressure (17%), grandmother’s opinion (50%) and mother’s own decision (33%). As concerns the recommendations given in the NCG, 23 mothers (60.5%) reported that they were very good, 14 mothers (36.8%) that they were good, and one mother reported that they were not helpful. The educational material given was considered understandable and practical for all the mothers. At 12 mo, 31 NGG mothers (83.8%) reported that they could afford to include red meat $3 times/wk, whereas 6 mothers found it too expensive to include red meat, and 1 mother did not give a response. One-hundred percent of mothers in the NGG reported that their infants tolerated meat and all kinds of red meat offered, and there were no adverse effects (in terms of gastrointestinal symptoms such as distress or vomiting) of consuming these foods during the whole period of intervention. Intake of recommended foods There was no significant difference between groups in the proportion of infants who consumed meat, red meat, or fruit at baseline (Figure 2, Tables 2 and 3). At 12 mo of age, infants in the NGG were significantly more likely to have daily consumption of meat, red meat, fruit, and vegetables, whereas infants in the CG were significantly more likely to have daily consumption of follow-on formula and cow milk. The frequency of red meat consumption per week was significantly greater in the NGG over the whole intervention period. The mean number of portions of meat, red meat, fruit, vegetables, and legumes

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)

No. of breastfeeds/d Time/breastfeed (min) No. of breastfeeds/night Breast milk intake (mL)

3.7 16.12 2.08 450.7

1

6 6 6 6

2.33 9.6 1.79 209.3

CG, control group; NGG, new guidelines group. All values are means; 95% CIs in parentheses. 3 Mean 6 SD (all such values). 2

CG (n = 38)

Difference2

6 6 6 6

20.18 (21.17, 0.82) 20.96 (25.4, 3.47) 20.26 (21.01, 0.56) 250.9 (2142.1, 40.4)

3.9 17.13 2.35 501.5

1.95 8.9 1.7 171.5

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the CG)] Surprisingly, 23.8% of infants in the NGG and 16.3% of infants in the CG were already consuming cow milk at 6 mo of age. To prevent iron and vitamin A deficiency, the Colombian government recommends iron supplementation [2 mg/kg weight (38)] and vitamin A supplementation [100,000 UI (39)] at 6 and 12 mo of age. However, compliance with iron and vitamin A supplements was very low; 4 infants (10.8%) in the NGG and 6 infants (15.8%) in the CG received a first dose of iron at 6 mo of age; 3 infants (7.9%) in the CG and no infants (0%) in the NGG received the second dose at 12 mo of age. Four infants (10.8%) in the NGG and 7 infants (18.4%) in the CG received vitamin A supplementation at 6 mo of age, and 2 infants (5.4%) in the NGG and 4 infants (10.8%) in the CG received the second dose at 12 mo of age.

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OLAYA ET AL TABLE 3 Comparison of feeding practices at 12 mo of age between the NGG and CG by using data from a food-frequency questionnaire and 24-h recall1 Variable

NGG (n = 38)

P

29 19 28 37 35 27

(76.3) (50.0) (73.7) (97.4) (92.1) (71.1)

32 31 17 25 22 11

(84.2) (83.8) (45.9) (67.6) (59.5) (29.7)

0.39 0.002 0.014 0.001 0.001 0.001

28 37 27 35 23

(73.7) (97.4) (71.1) (92.1) (69.5)

17 25 11 22 16

(45.9) (67.1) (29.7) (59.5) (43.2)

0.01 0.001 0.001 0.001 0.13

1

CG, control group; NGG, new guidelines group. Milk refers to any other milk than breast milk (ie, follow-on formula and cow milk). 3 Recommended food groups and frequencies: meat, 5 times/wk; red meat, 3 times/wk; vegetables, 7 times/wk; fruit, 7 times/wk; and legumes, 3 times/wk. 2

consumed per week was also significantly higher in the NGG, whereas infants in the CG consumed significantly more portions per week of sweetened foods (defined as sugar, jelly, chocolate, and sweets), milk, and cow milk (Figure 2). Significantly more infants in the NGG consumed recommended food portions per week at 12 mo of age, whereas infants in the CG had significantly more bottle-feeds than those of infants in the NGG, consumed cow milk more than 1 time/wk, and had ,2 main meals/d There was no significant difference between groups in the number of breastfeeds per day, time per breastfeed, and number of breastfeeds per night. Linear growth The length-for-age z score (LAZ) at 6 and 12 mo of age and the change in LAZ were not significantly different between groups (Table 4). The number and proportion of infants with a LAZ less than 22 SDs was significantly higher at 6 mo of age in the NGG [10 infants (23.8%)] than in the CG [2 infants (4.7%)] (P = 0.02). At 12 mo of age, there was no significant difference between groups, but the number and proportion of infants with a LAZ less than 22 SDs in the CG increased from 2 infants (4.7%) at 6 mo of age to 8 infants (21.1%) at 12 mo of age, whereas the number and proportion in the NGG remained similar at 12 mo of age to those at 6 mo of age. After adjustment for baseline LAZ and socioeconomic factors, the change in LAZ from 6 to 12 mo of age was not predicted by the randomly assigned group, and there was no interaction between the LAZ at 6 mo of age and the randomly assigned group on the change in LAZ from 6 to 12 mo of age (P = 0.9). Iron status Values of hemoglobin, hematocrit, MCV, and SF at 6 and 12 mo of age and the change between 6 and 12 mo of age for the NGG and CG are shown in Table 5. At 6 mo of age, there was no significant difference in these indicators between groups. Hemoglobin (P = 0.009) and hematocrit (P = 0.02) were significantly

higher in the NGG than CG at 12 mo of age. These differences remained after adjustment for confounding factors such as sex, birth weight ,3 or $3 kg, weight gain from 0 to 6 mo of age, and weight at 6 mo of age. SF at 12 mo of age was not significantly different between groups, and this finding was unchanged when 5 infants (2 infants in the NGG and 3 infants in the CG) with CRP .6 were excluded from the analysis. Changes in hemoglobin and hematocrit from 6 to 12 mo of age were positive and were significantly higher in the NGG than CG [mean 6 SD change in hemoglobin 0.41 6 0.8 g/dL compared 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 socioeconomic factors, the change in hemoglobin from 6 to 12 mo of age was negatively predicted by the hemoglobin at 6 mo of age (coefficient: 20.58; 95% CI: 20.82, 20.33; P # 0.001), and there was a positive effect of the randomly assigned group (coefficient: 0.56; 95% CI: 0.19, 0.92; P = 0.003). There was no interaction between hemoglobin at 6 mo of age and the randomly assigned group on the change of hemoglobin from 6 to 12 mo of age (P = 0.42). The change in hematocrit from 6 to 12 mo of age was not related to baseline hematocrit after adjustment for socioeconomic factors, and there was no interaction between hematocrit at 6 mo of age and the randomly assigned group on the change in hematocrit from 6 to 12 mo of age (P = 0.73). SF decreased from 6 to 12 mo of age in both groups with no significant difference between groups (227.23 6 44.8 mg/L in the CG compared with 213.62 6 37.3 mg/L in the NGG; 95% CI for difference in decline: 20.63, 33.5; P = 0.2). After adjustment for socioeconomic factors, baseline SF was not associated with the change in SF from 6 to 12 mo of age, and there was no interaction between SF at 6 mo of age and the randomly assigned group on the change in SF from 6 to 12 mo of age (P = 0.64). The proportion of infants who had a hemoglobin concentration ,11 g/dL and hematocrit ,33% at 12 mo of age was 4 infants (11%) in the CG and 0 infants (0%) in the NGG (P = 0.1). The

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Proportion of infants consuming selected food groups daily [n (%)] Dairy products (yogurt, cheese) Milk2 Meat Red meat Fruit Vegetables Proportion of infants consuming selected recommended food groups at the recommended frequency [n (%)]3 Meat (all types) Red meat Vegetables Fruit Legumes

CG (n = 38)

1 Anthropometric data at 6 mo of age are shown for those infants who also had measurements at 12 mo of age. a,bStudent’s t test: aP , 0.05, bP , 0.01. CG, control group; HCZ, head circumference–for-age 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. 2 All values are means; 95% CIs in parentheses. 3 Mean 6 SD (all such values).

0.18 (20.02, 0.39) 0.13 (20–16, 0.43) 0.09 (20.23, 0.42) 0.11 (20.09, 0.31) 0.059 (20.26, 0.38) 0.44 0.67 0.66 0.3 0.71 6 6 6 6 6 20.19 20.27 20.26 20.006 0.28 0.45 0.60 0.76 0.52 0.70 6 6 6 6 6 20.00 20.13 20.16 0.11 0.34 0.00)a 0.39) 20.12)b 0.28) 0.00)a -0.64 (21.0, 20.2)a 20.23 (20.7, 0.23) 20.63 (21.1, 20.20)a 20.26 (20.64, 0.12) –0.47 (20.9, 20.06)a 6 6 6 6 6

0.93 1.1 0.84 0.80 0.8 20.59 20.98 0.12 0.08 0.22 WAZ LAZ WLZ HCZ MUACZ

0.06 20.76 0.76 0.34 0.69

1–0 0.9 1.0 0.87 0.9 6 6 6 6 6

20.59 21.12 20.043 0.18 0.55

6 6 6 6 6

0.9 1.1 0.9 0.91 0.9

20.12 21.02 0.49 0.33 0.97

6 6 6 6 6

1.0 1.0 1.0 0.9 0.9

20.46 20.98 –0.54 20.15 20.42

(20.93, (20.59, (20.96, (20.57, (20.84,

CG (n = 38) NGG (n = 38) Difference2 CG (n = 38) NGG (n = 38) Difference2 CG (n = 38) NGG (n = 38) Variable

12 mo of age 6 mo of age

TABLE 4 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

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proportion of infants with a SF concentration ,12 mg/L at 6 mo of age was significantly higher [5 infants (12.2%)] in the NGG] 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. The mean increase was higher in the CG than in the NGG, but there was no significant difference between groups [mean 6 SD change: 31.01 6 25.7 mg/dL in the CG compared with 20.33 6 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 at 6 mo of age compared with 1 6 2.9% in the CG; and 1 6 2.9% in the NGG compared with 0 6 0% in the CG at 12 mo of age; NS]. Other anthropometric variables The WAZ was significantly higher at baseline in CG than in NGG infants, and similar results were observed for the WLZ and MUACZ at both 6 and 12 mo of age. However, changes in the WAZ, WLZ, head circumference–for-age z score, and MUACZ from 6 to 12 mo of age were not significantly different between groups (Table 4). After adjustment for baseline differences, the WAZ at 12 mo of age was strongly related to the WAZ at 6 mo of age (coefficient: 0.946; 95% CI: 0.83, 1.057; P = 0.0001). When socioeconomic factors and sex were included in the model with randomly assigned groups by using stepwise regression models, the WAZ at 6 mo of age remained related to the WAZ at 12 mo of age, with no significant effect of the randomly assigned group. Similar results were shown for the WLZ and MUACZ at 12 mo of age. After adjustment for socioeconomic factors, neither baseline values nor randomly assigned group were significant predictors of changes in the WAZ or WLZ from 6 to 12 mo of age, and there were no significant interactions between baseline measurements and randomly assigned groups. Similar results were shown for the change in MUACZ from 6 to 12 mo of age. Meat intake and iron and zinc status After adjustment for socioeconomic factors, the frequency (number of times per week) of red meat consumption from 8 to 10 mo of age was positively correlated with hemoglobin (r = 0.25, P = 0.03) and hematocrit (r = 0.27, P = 0.02) at 12 mo of age. The same positive correlation for this period was observed with changes in hemoglobin, hematocrit, and SF. The frequency of red meat consumption from 6 to 8 mo of age also showed a positive correlation with the change in hemoglobin from 6 to 12 mo of age (r = 0.24, P = 0.05; Table 6). Infants with red meat consumption $3 times/wk from 6 to 8 mo of age had significantly higher MCV at 12 mo of age than did infants with red meat consumption ,3 times/wk (72.5 6 4.4 fL) compared with 69.6 6 3.7; P = 0.02 ]and a greater increase in MCV from 6 to 12 mo of age (P , 0.05), whereas infants with red meat consumption $3 times/wk from 10 to 12 mo of age had higher hemoglobin concentrations (P = 0.016) and hematocrit (P = 0.03) at 12 mo of age and a significantly greater increase in hemoglobin from 6 to 12 mo of age (P , 0.01).

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Change from 6 to 12 mo

Difference2

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1 Data at 6 mo of age are shown for infants who also had measurements at 12 mo of age. guidelines group. 2 All values are means; 95% CIs in parentheses. 3 Mean 6 SD (all such values).

0.003 (20.34, 0.34) 0.03 (20.89, 0.95) 20.06 (21.66, 1.54) 24.69 (221.8, 12.4) 3.65 (28.8, 16.0) 12.1 35.7 71.4 38.7 92.4

0.73 1.9 3.8 30.3 29.7

12.1 35.6 71.4 43.4 88.7

0.8 2.1 3.1 40.5 19.3 6 6 6 6 6 6 6 6 6 6 Hemoglobin (g/dL) Hematocrit (%) MCV (fL) Ferritin (mg/L) Zinc (mg/dL)

36 36 36 34 34

12.5 36.6 72.4 23.7 110.6

6 6 6 6 6

0.7 1.9 3.9 22.3 34.0

a,b

Student’s t- test: aP , 0.05, bP , 0.001. CG, control group; MCV, mean corpuscular volume; NGG, new

(0.11, 0.9)b (0.12, 2.3)a (20.42, 3.0) (26.3, 33.5) (227.0, 5.7) 0.5 1.2 1.3 13.6 210.7 6 6 6 6 6 20.13 20.15 20.20 227.2 31.0 37 37 37 35 37

11.9 35.5 71.4 17.3 114.9

6 6 6 6 6

0.9 2.1 4.8 14.7 23.1

0.52 1.13 0.97 6.31 24.23

(0.13, 0.9)b (0.19, 2.1)a (21.08, 3.0) (22.7, 15.4) (217.9, 9.4)

36 36 36 33 32

0.41 1.04 1.07 213.6 20.3

6 6 6 6 6

0.8 2.2 3.3 33.8 37.3

37 37 36 30 30

CG n NGG n Difference2 CG n NGG Difference2 CG (n = 38) NGG (n = 38) Variable

n

12 mo of age 6 mo of age

TABLE 5 Comparison of iron and zinc status at 6 and 12 mo of age and the change from 6 to 12 mo of age between randomly assigned groups1

There was no correlation between the mean frequency of red meat consumption per week and serum zinc at 12 mo of age or the 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 10 to 12 mo of age had significantly greater increase in zinc between 6 and 12 mo of age. DISCUSSION

The new CF guidelines tested in this trial were designed to provide clear, specific, and practical advice for mothers living in poor socioeconomic conditions in Bogota. The guidelines were developed following WHO 2003 recommendations (12) but also by taking into account the findings from our earlier studies that described current CF practices in Bogota so that the guidelines would be acceptable in terms of culture and food availability. The 3 main messages, emphasized at each study visit, both verbally and in writing, emphasized the importance of 1) continuing breastfeeding alongside CF, 2) red meat as a source of iron and zinc, and 3) fruit and vegetables. Our preliminary results confirmed the feasibility of the intervention; the new guidelines were acceptable and affordable by the majority of mothers, despite living in conditions of socioeconomic constraint. Efficacy was also shown with improved consumption of red meat, fruit, and vegetables. The transition to CF was successfully attained by infants in the NGG who, compared with infants in the CG, had a better meal pattern and feeding practices including a lower consumption of cow milk and formula with less bottlefeeds and consumption of sweetened foods. The intervention had no adverse effect on breastfeeding, which was consistent with results from cluster randomized studies of interventions to improve CF practices in Malawi (21) and China (24). The intervention was associated with evidence of improved iron status, with higher hemoglobin and hematocrit and positive changes in hemoglobin and hematocrit from 6 to 12 mo of age. Although there was no effect of the intervention on SF, the frequency of red meat consumption from 8 to 10 mo of age was positively associated with the change in SF from 6 to 12 mo of age. We could not directly compare our findings with those from other studies which have used supplementation or interventions with meat or a combination of nutrition education with recommendations to improve CF. We gave specific advice on the type, amount, and frequencies of foods to be given to the infant together with education on the importance of certain foods; however, foods were not provided because we considered that this approach would have a greater likelihood of a sustained impact on nutritional intakes and dietary habits. Previous randomized controlled trials (RCTs) (28, 29, 40) that investigated meat or red meat consumption were conducted in developed countries, and meat was provided during the period of intervention. One study reported an effect of higher meat intake on hemoglobin but not on SF, which was consistent with our findings, whereas a study in German infants showed that the consumption of commercial weaning foods with a low meat content increased risk of developing marginal iron status at 10 mo of age in infants who were exclusively breastfed for 4–6 compared with the consumption of weaning foods with a higher meat intake (40). A longitudinal cohort study in the United Kingdom (41) also reported that a higher meat intake during the first year was associated with a higher hemoglobin concentration. Some cluster randomized

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Change from 6 to 12 mo

1.0 2.4 3.9 44.8 25.7

Difference2

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EFFICACY OF NEW COMPLEMENTARY FEEDING GUIDELINES TABLE 6 Unadjusted correlations between frequency (mean no. of times/wk) of red meat consumption and change in iron status from 6 to 12 mo of age1 Variable

Change in hematocrit from 6 to 12 mo of age

Change in MCV from 6 to 12 mo of age

Change in SF from 6 to 12 mo of age

70 0.24 0.05

70 0.16 0.20

69 0.12 0.34

61 0.07 0.56

73 0.32 0.006

73 0.34 0.003

72 0.11 0.34

63 0.30 0.02

72 0.21 0.07

72 0.18 0.13

71 0.063 0.60

62 0.14 0.29

73 0.307 0.008

73 0.27 0.02

72 0.11 0.345

63 0.15 0.23

1 r, Pearson’s correlation coefficient for changes in hemoglobin, hematocrit, and MCV and Spearman’s correlation for changes in SF. MCV, mean corpuscular volume; SF, serum ferritin.

trials that used nutrition education combined with recommendations to improve CF (21–27) have reported significantly increased meat consumption but did not focus on the effect of meat consumption on iron and zinc status. Other strategies such as iron supplementation and sprinkles have been used to improve iron status in infants with conflicting results, and RCTs that used sprinkles were generally testing the treatment rather than primary prevention (20, 42). In a blinded RCT in Honduras and Sweden, iron supplementation from 4 to 9 mo of age resulted in a significant increase in hemoglobin and reduced iron deficiency anemia in Honduras but not in Sweden (16), where impaired linear growth was observed (17). A study in Indian infants also reported a negative effect of iron supplementation on growth (43). In addition, compliance with iron supplementation is often very low (15, 44). We showed no significant effect of the intervention on zinc status at 12 mo of age or a change in zinc status from 6 to 12 mo of age. Serum zinc concentrations increased in both groups and were not correlated with the frequency of red meat consumption per week, which were results similar those in a randomized trial of meat compared with micronutrient fortified cereals in US infants (28). However, we showed that those infants who ate red meat ,3 times/wk had greater and more-positive changes in zinc status compared with those who ate red meat more frequently, which suggested potential negative effects of increased red meat consumption on zinc status. It is plausible that iron in red meat could interfere with zinc absorption. However, there is a need for additional research in this area to examine interactions between iron and zinc intakes during CF. The intervention had no significant effect on anthropometric measures at 12 mo of age or on changes in z scores between 6 and 12 mo of age. A greater proportion of infants in the NGG had linear stunting at 6 mo of age, but because this proportion did not increase by 12 mo of age in the NGG, whereas it increased

in the CG, suggested a possible protective effect of the intervention. Our findings were in agreement with those from 3 RCTs that investigated meat as a CF food, albeit by using different indicators (28, 29, 40), and with those from a cluster randomized study in Pelotas, Brazil (26). Conversely, studies in Pakistan (25), China (23), and Peru (22) reported positive effects of interventions on growth. Although the approach used to deliver the messages recommended in the new CF guidelines was feasible and successful in the setting of this study, the implications in terms of staffing and resources need to be evaluated before the guidelines can be more widely used. The messages were delivered by researchers, and each session lasted w45 min, which was longer than the time currently allocated for routine clinic visits. It would also be important to examine in more detail which parts of the guidelines and their delivery were most important for success because this might allow them to be implemented in a more-efficient way. This issue was not examined in this study, but several of the following possible factors may have contributed to the effective uptake of the guidelines: 1) the guidelines were designed on the basis of local culture, food availability, environment, and infant characteristics; 2) individual counseling sessions allowed educational messages to be adapted to individual needs and understandings; 3) the 3 main messages were repeated and reinforced by written materials; and 4) emphasis was given to the importance of the recommendations for the infant’s health. Our observation that grandmothers played an important role in the feeding decisions of mother suggested that it might be worth including this group in any future intervention. The main strength of the study was the randomized design, which allowed for causal relations between the intervention and outcomes to be established. Compliance with the protocol was good, and there was low attrition. The main limitation of the study was the relatively small sample size, which limited the power for

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Frequency of red meat/wk from 6 to 8 mo of age n r P Frequency of red meat/wk from 8 to 10 mo of age n r P Frequency of red meat/wk from 10 to 12 of age n r P Frequency of red meat/wk from 6 to 12 mo of age n r P

Change in hemoglobin from 6 to 12 mo of age

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OLAYA ET AL

We thank the mothers and infants who participated in the study and the staff in Fontibon and Suba Hospitals who helped during the period of data collection. We also thank Angela Uman˜a (Research Office at the Pontificia Universidad Javeriana, Bogota, Colombia), Ingrid Schuller (Faculty of Sciences, Pontificia Universidad Javeriana), and Wilson Mejia for supporting the submission of the project at the Pontificia Universidad Javeriana; Maria del Pillar Rodriguez (Nutrition Department, Suba Hospital) and Cristina Mendez (Suba Hospital) for helping with study preparations in the hospitals; and Luisa Fernanda Tovar (Nutrition and Biochemistry Department) for her contribution with taking pictures of CFs used in the brochures and all educational material developed for the study, We also thank JAVEGRAF (Pontificia Universidad Javeriana) for their contribution in the designing and printing of the educational material, Maria Fernanda Ramirez and Luz Marina Fernandez of the laboratory in the Suba Hospital for undertaking the biochemical analyses, and Deisy Fonseca for her help in data collection. The authors’ responsibilities were as follows—GAO: study concept and design, design of new CF guidelines, conduction of the study, statistical

analyses, manuscript writing, and critical reading of the manuscript; and ML and MSF: design of new CF guidelines and trial, data interpretation, and critical reading and revision of manuscript. None of the authors declared a conflict of interest following the guidelines of the International Committee of Medical Journal Editors.

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some analyses. With 38 subjects per group, we had 80% power to detect a difference of a 0.69 SD at 5% significance and could have missed a smaller, although perhaps clinically relevant, effect on outcomes. The small sample size also resulted in a baseline imbalance in anthropometric measures between groups, which we addressed by comparing differences in outcome variables adjusted for the baseline value and testing for interactions between the baseline value and randomly assigned group. We chose not to impute missing outcome data, and this may have introduced some bias, although when we compared baseline characteristics by group, the only difference was baseline differences in WAZ, WLZ, and MUACZ were significant for all infants randomly assigned but not for those with follow-up data. We made no formal statistical correction for the multiple comparisons made during the study, and the possibility that this lack resulted in a type II error with significant differences apparent due to chance should be considered when interpreting the findings. Also, the study was also not blinded, which may have influenced certain outcomes such as dietary intakes and anthropometric measures, although this was unlikely because the laboratory measurements as blood sampling and analyses were performed by staff with no connection to the study or knowledge of the protocol. Finally, infants were not followed beyond the period of intervention, and thus, we could not investigate the sustainability of the observed effects. In conclusion, these preliminary data suggest that the use of CF guidelines emphasizing red meat consumption might be a practical strategy for improving both CF practices and iron status, especially in countries such as Colombia where many strategies aimed at improving iron status have already been tried without great success. Theoretically, red meat may be a good first complementary food for all breastfed infants, regardless of their environment, although this strategy would not be suitable in all settings. A larger trial would be needed to evaluate the new CF guidelines in other settings to test the generalizability and potential for adapting the guidelines according to local circumstances. Such a trial should have a sufficient sample size to allow subgroup analyses according to sex and mode of feeding before 6 mo of age to detect smaller differences in outcome measures between groups and to further investigate associations between meat intake and measures of iron status. Ideally, a longer followup should be incorporated to examine whether dietary effects of the intervention are maintained and associated with longer-term effects on outcomes such as growth and developmental outcomes.

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Efficacy and safety of new complementary feeding guidelines with an emphasis on red meat consumption: a randomized trial in Bogota, Colombia.

Iron deficiency and poor linear growth are common in infants from deprived socioeconomic backgrounds and may be associated with inadequate complementa...
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