The Journal of Nutrition

Community and International Nutrition

Dietary Diversity at 6 Months of Age Is

Associated with Subsequent Growth and
Mediates the Effect of Maternal Education on
Infant Growth in Urban Zambia1,2
Simonette R. Mallard,3* Lisa A. Houghton,3 Suzanne Filteau,4 Anne Mullen,5 Johanna Nieuwelink,4
Molly Chisenga,6 Joshua Siame,6 and Rosalind S. Gibson3

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3
Department of Human Nutrition, University of Otago, Dunedin, New Zealand; 4Department of Epidemiology and Population Health,
London School of Hygiene and Tropical Medicine, London, UK; 5Diabetes and Nutritional Sciences Division, KingÕs College School of
Medicine, London, UK; and 6University Teaching Hospital, Lusaka, Zambia

Abstract
Background: Although numerous cross-sectional studies have shown an association between WHO infant and young
child feeding (IYCF) indicators and child anthropometric measures, limited longitudinal evidence exists linking these
indicators with subsequent growth.
Objectives: The purpose of this study was to investigate whether meeting WHO IYCF indicators at 6 and 12 mo of age
was associated with growth to 18 mo of age and if dietary diversity mediated the relation between household wealth,
maternal education, and child growth.
Methods: We used longitudinal data on 811 infants in the CIGNIS (Chilenje Infant Growth, Nutrition, Infection Study), a
randomized controlled trial comparing the effect of micronutrient-fortified porridges on infant growth in Lusaka, Zambia.
Twenty-four–h diet recalls were conducted at 6 and 12 mo of age, and length and weight measurements at ages 6 and
18 mo were used to produce height-for-age Z-scores (HAZs) and weight-for-height Z-scores (WHZs). Information on
household assets was used to generate a household wealth index, and level of maternal education was collected.
Results: In fully adjusted analyses, iron-rich food intake at 6 mo and greater household wealth and maternal education
were positively associated with HAZ at 18 mo (all P # 0.016). Iron-rich food intake at 6 and 12 mo, achieving a ‘‘minimum
acceptable diet’’ at 12 mo, and higher maternal education were associated with greater WHZ at 18 mo (all P # 0.044).
Dietary diversity at 6 mo of age was positively associated with both HAZ and WHZ at 18 mo (both P # 0.001) and mediated
13.4% and 25.9% of the total effect of maternal education on HAZ and WHZ, respectively, at 18 mo.
Conclusions: Our findings indicate that IYCF programs should be targeted toward the early period of complementary
food introduction and that policies aimed at increasing formal maternal education may benefit child growth through
improved feeding practices. This trial was registered at www.controlled-trials.com as ISRCTN37460449. J. Nutr.
144: 1818–1825, 2014.

Introduction
Worldwide, nearly half of all mortality among infants and children
<5 y of age is related to malnutrition, accounting for 3.1 million
deaths annually (1). Resource-constrained countries bear the
majority of this burden; in the sub-Saharan nation of Zambia,
;12% of all children die before their fifth birthday, with malnu-
trition estimated to be implicated in 42% of these deaths (2,3).
Infant and young child feeding (IYCF)7 practices directly
affect the nutritional status of children and consequently impact
1
Supported by Bill and Melinda Gates Foundation grant 37253 and Sight and
Life, Basel, Switzerland.
2
Author disclosures: S. R. Mallard, L. A. Houghton, S. Filteau, A. Mullen,
J. Nieuwelink, M. Chisenga, J. Siame, and R. S. Gibson, no conflicts of interest.
* To whom correspondence should be addressed. E-mail: simonette.mallard@
otago.ac.nz.
child morbidity and mortality (4). Population-based indicators
used to monitor the adequacy of breastfeeding practices were
first established by the WHO in 1991 (5), and in 2008 the
indicators were extended to include complementary feeding
practices (4). Collectively termed ‘‘infant and young child
feeding’’ indicators, these optimal feeding practices were iden-
tified from 10 studies in Africa, Asia, and Latin America (6).
Although intended for assessing the adequacy of infant feeding
practices at the population level, numerous researchers have
7
Abbreviations used: CIGNIS, Chilenje Infant Growth, Nutrition, Infection Study;
HAZ, height-for-age Z-score; IYCF, infant and young child feeding; MAD,
minimum acceptable diet; MDD, minimum dietary diversity; MMF, minimum
meal frequency; SEP, socioeconomic position; VIF, variance inflation factor;
WHZ, weight-for-height Z-score.

ã 2014 American Society for Nutrition.

1818 Manuscript received July 3, 2014. Initial review completed August 4, 2014. Revision accepted August 18, 2014.
First published online September 3, 2014; doi:10.3945/jn.114.199547.
linked meeting IYCF indicators with a reduction in growth
faltering at the individual level by using regression modeling (7–
14). In most cases, these associations were based on cross-
sectional studies (7–11), so inferences of causation cannot be
made, although a small number were derived from longitudinal
studies by generating summary scores of IYCF indicators (12–
14). Establishing relations between IYCF indicators and subse-
quent growth on the basis of longitudinal data is valuable for the
development of nutrition interventions and for convincing
policymakers and nongovernmental organizations of the impor-
tance of promoting and facilitating appropriate complementary
feeding practices.
The objective of the current study was to extend the growing
body of evidence linking IYCF practices with subsequent growth
by using a large, longitudinal data set from urban Zambia, by
examining the relation between complementary feeding practices
of infants at 6 and 12 mo of age and their growth up to 18 mo of
age. Target nutrient and energy densities, i.e., nutrient intakes per
100 kcal and energy intake per gram of food, are highest for
infants aged 6 to 8 mo because of their limited gastric capacity
(249 vs. 345 g/meal at 12 mo of age) (15). However, these targets
are often not achieved because of the poor bioavailability and
inadequate nutrient and energy density of many plant-based
complementary foods commonly used in resource-constrained
countries (16). Therefore, we hypothesized that IYCF practices,
particularly dietary diversity, an indicator of micronutrient
adequacy, may be more critical for the subsequent growth of
infants at 6 mo than at 12 mo of age. Socioeconomic position
(SEP) is known to influence both childhood growth (17,18) and
dietary diversity (19–22). Concurrent with the primary objective,
we therefore investigated whether dietary diversity played a
mediating role in the association between SEP, as measured by
maternal education and an asset-based index of household
wealth, and infant growth.
Participants and Methods
Study design and population. The Chilenje Infant Growth, Nutrition,
and Infection Study (CIGNIS) was a randomized controlled trial, the
details of which were previously described (23). Briefly, CIGNIS was
conducted in Chilenje, a middle-income area of Lusaka, Zambia, from
October 2005 to July 2009. Zambia is an HIV-endemic area, and
within Zambia, Lusaka had the highest HIV prevalence in 2007
among reproductive-aged women (22.4%) (3). All women attending
the local government health clinic for monthly infant growth monitoring
or early vaccinations were informed of the study, accounting for >90%
of all new mothers in the catchment area (24). Infants were eligible for
inclusion if they were aged 6 mo 6 2 wk and had no evidence of severe
disease. Eligible infants whose parents or guardians gave written
informed consent were randomly assigned to consume for 1 y either a
richly micronutrient-fortified porridge targeted to meet the needs of
infants or a basal porridge fortified at proposed national maize flour
fortification levels. The 2 porridges were based on maize, beans,
Bambara nuts, and groundnuts and were similar in bulk ingredients
and macronutrient content, with an energy density of 414–420 kcal/g,
but differed in micronutrient content. Of the infants enrolled, 68 were
inadequately randomized due to a shortage of 1 of the porridges at the
time of their recruitment; these infants were not excluded from our
analyses because randomization was not a requirement of the current
study.
Ethics. The Human Ethics Committees of the University of Zambia and
the London School of Hygiene and Tropical Medicine approved the
study protocol. All mothers gave informed written consent. For ethical
reasons, all infants in the trial were supplemented with vitamin A
capsules at their 6-, 12-, and 18-mo clinic visits, according to the
standard protocol of care, through the government national vitamin A
supplementation program.
Anthropometric measures. Weight and length were measured at the
study clinic every 3 mo by trained anthropometrists with children
unclothed or wearing a diaper with the use of standardized techniques
and calibrated equipment, as described in detail elsewhere (23). A digital
balance (to 10 g) and length board (to 1 mm) were used for infant weight
and length, respectively (all anthropometry equipment was from
Chasmor). The precision of the anthropometric measurements was
good, as indicated by inter- and intraexaminer technical error of the
measurements (25). Maternal height was measured at recruitment by
using a wall-mounted microtoise tape (to 1 mm). All measurements were
performed in triplicate, and the median was used in analyses. Height-for-
age Z-scores (HAZs) and weight-for-height Z-scores (WHZs) were
generated by using the most recent WHO growth reference data macros
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for Stata (26).
Dietary IYCF indicators. Trained research assistants conducted single
24-h dietary recalls in the homes with the caregiver of each child by using
the interactive, multiple-pass technique at baseline before treatment
initiation and at 6-mo intervals thereafter (27). Data from interviews at 6
and 12 mo of age were used in the current study. For actual portions of
porridges consumed by the infants, caregivers were requested to spoon
the portions consumed by their child into the childÕs bowl or graduated
plastic feeding cup (graduated in milliliters) provided by the investiga-
tors, which was then weighed on dietary scales (Soehnle; CMS Weighing
Equipment). Portion sizes of other foods consumed were determined by
calibrating utensils used in the home with the use of graduated
measuring cylinders, cups, or spoons. For composite dishes, household
recipe data were collected (27).
Dietary diversity was calculated by summing the reported number of
food groups consumed in the 24-h recall period. Seven food groups were
defined in accordance with WHO specifications: 1) grains, roots, and
tubers; 2) legumes and nuts; 3) dairy products (milk, yogurt, cheese); 4)
eggs; 5) flesh foods (meat, fish, poultry, and liver/organ meats); 6)
vitamin A–rich fruits and vegetables; and 7) other fruits and vegetables
(28). All food groups contained in a mixed dish were counted separately.
Condiments and clear broths from simmered dishes and soups were not
included in dietary diversity counts. ‘‘Minimum dietary diversity’’
(MDD) was defined as having reported consumption of $4 food groups
in the 24-h recall period.
‘‘Minimum meal frequency’’ (MMF) for breast-fed infants at 6 mo of
age was defined as having consumed $2 solid, semisolid, or soft meals on
separate occasions in the 24-h recall period and $3 meals at 12 mo of age.
For non–breast-fed infants, a minimum of $4 meals was required at both
6 and 12 mo, including at least 2 animal-source milk feedings. For both
breast-fed and non–breast-fed infants, ‘‘meals’’ included both meals and
snacks other than trivial amounts (<10 g). Clear broths from simmered
dishes and soups were not regarded as solid, semisolid, or soft foods.
‘‘Minimum acceptable diet’’ (MAD) was defined as meeting the
requirements for both MDD and MMF for breast-fed infants. To avoid
the double counting of milk feedings, non–breast-fed infants who
consumed both the MDD (not including milk feedings) and the MMF
during the 24-h recall period met the requirements for MAD, as specified
by the WHO (28).
‘‘Consumption of iron-rich or iron-fortified foods’’ was defined as
having consumed a flesh food or an iron-fortified food specially
designed for infants and young children. The richly fortified inter-
vention porridge (but not the basal porridge) was fortified with iron
at amounts designed to meet the needs of infants; therefore, this
indicator differed depending on treatment allocation at the 12-mo
recall. All analyses controlled for treatment group. The indicator
‘‘introduction of solid, semisolid, or soft foods’’ was not assessed
because only 1 infant reportedly did not consume any of these foods in
the previous 24 h at baseline.
SEP. An asset-based index of household wealth was constructed as
previously described (29) by using the first axis of a principal compo-
nents analysis. Variables included the following: home ownership;
Dietary diversity predicts subsequent infant growth 1819
sanitation facilities; floor type; connection to water, electricity, and
telephone; number of meals per day; transport type; and ownership of
electrical appliances, animals, and a vegetable garden. This continuous
index was then divided into quintiles from lowest to highest household
wealth. Maternal education was categorized as primary school or less,
secondary school, and college/university.
Morbidity, HIV exposure, and iron status. At scheduled and
unscheduled clinic visits, basic care plus prescription of antibiotics or
antimalarial drugs were accessible. For other treatments, infants were
referred either to the Chilenje main clinic or to the University Teaching
Hospital, the local tertiary facility. Information about diagnoses and
treatments in the hospital was available to the CIGNIS project. Data on
hospital admissions before age 6 mo were not collected, although at the
time of recruitment eligible infants had no evidence of severe disease. For
modeling the compliance with the WHO IYCF indicators at 12 mo on
tested HIV positive at 18 mo of age. All analyses were conducted by using
Stata 11.2, and a 2-sided 0.05 level of significance was used in all cases.
Results
A total of 811 infants were recruited at baseline, comprising
62% of all those eligible and 44% of all those screened (Table 1).
Loss to follow-up at 18 mo was 22% of all infants recruited;
reasons for withdrawal did not differ by household wealth
quintile or maternal education (23). Nine percent of all mothers
did not know or did not wish to disclose their HIV status, and
24% of all remaining women were HIV-positive. Twelve
children died during the study, 8 of whom had HIV-infected
mothers, and 17 children tested HIV-positive at 18 mo. One-

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third (33%) of mothers had an educational level of primary
subsequent growth, hospital admission between 6 and 12 mo (never or
ever) was included as a measure of serious illness that may affect growth. school or below, a little over one-third had achieved secondary
Admissions for planned surgeries (circumcision and congenital anoma- school education (38%), and the remaining women (29%) had
lies) were excluded. At each scheduled 3-monthly anthropometric clinic attained college or university qualifications. The prevalences of
visit, mothers also reported on recent infant morbidity (past 3 d) and stunting and wasting among infants at 6 mo were 12% and 3%,
morbidity since the previous visit (past 3 mo). Because of its known respectively. Stunting at 12 and 18 mo increased to 14% and
negative effect on growth (30), reported diarrhea (at least 3 loose stools 20%, respectively, whereas wasting remained relatively stable at
or 1 bulky watery stool in a 24-h period) was included as a covariate in 5% and 3%, respectively.
statistical modeling. Diarrhea in the past 3 mo at the baseline clinic visit In analyses adjusted only for baseline anthropometric mea-
was included in models of 6-mo data and the proportion of 3-monthly surements, greater household wealth and maternal education
clinic visits at which diarrhea was reported from 6 to 12 mo was included
were positively associated with HAZ and WHZ at 18 mo (all
in 12-mo models.
Maternal HIV status was determined on the basis of results from P # 0.001 for linear trend) (Table 2). The positive association
antenatal HIV antibody testing in the government health service. between both household wealth and maternal education and
Infant HIV status was determined at 18 mo of age by using an HIV HAZ at 18 mo remained significant when analyses were adjusted
antibody serial testing algorithm (23). Infant HIV exposure (i.e., for all baseline covariates (both P # 0.001 for linear trend). In
maternal HIV status) was included as a covariate in analyses rather
than infant HIV status at 18 mo, because few children tested HIV
positive (n = 17) and the variable was collinear with infant HIV
exposure. For most outcomes, HIV-infected children did not differ TABLE 1 Maternal and infant characteristics at baseline1
from the other HIV-exposed children, suggesting late transmission.
Infant anemia was also included as a covariate using hemoglobin (g/L) Characteristics n or n/total n Value2
measured in finger-prick blood samples (Hemocue) at 6 mo and 12 mo
of age. Infant characteristics
Age, d 811 184 6 9
Statistical analyses. Multiple linear regression was used to determine Females, % 426/811 53
the association between HAZ and WHZ at 18 mo (dependent variables) Birth weight, kg 800 3.05 6 0.49
and the following independent variables: household wealth; maternal Hemoglobin, g/L 811 107.8 6 12.8
education; WHO IYCF indicators at 6 and 12 mo (MDD, MMF, MAD,
Diarrhea in past 3 mo, % 164/810 20
and consumption of iron-rich/iron-fortified foods); consumption of
Height, cm 809 64.9 6 2.48
individual food groups at 6 and 12 mo; consumption of animal-source
foods (dairy products, flesh foods, or eggs) at 6 and 12 mo; and dietary HAZ 808 20.81 6 1.03
diversity score at 6 and 12 mo. All analyses using explanatory variables Stunting (,22 HAZ), % 808 12
at 6 mo of age controlled for 6-mo HAZ or WHZ, and all analyses using Weight, kg 811 7.28 6 1.08
explanatory variables at 12 mo of age controlled for 12-mo HAZ or WHZ 809 0.15 6 1.15
WHZ. Fully adjusted analyses included the following a priori con- Wasting (,22 WHZ), % 809 3
founders: hemoglobin at 6 or 12 mo, birth weight, maternal height, sex, HIV exposure, % 177/741 24
infant HIV exposure, diarrhea in past 3 mo (6-mo analyses) or Maternal characteristics
proportion of visits at which diarrhea was reported between 6 and Antenatal HIV status, %
12 mo (12-mo analyses), hospital admission between 6 and 12 mo
Negative 564/811 70
(12-mo analyses), treatment group, and household wealth and/or
Positive 177/811 22
maternal education. Multicollinearity of household wealth, maternal
education, and dietary diversity was assessed by using variance inflation Unknown 70/811 9
factors (VIFs) (31). Height, cm 810 159.7 6 6.00
Seemingly unrelated regression was used to estimate the indirect Education, %
effect of household wealth and maternal education that was mediated Primary school or less 269/811 33
through dietary diversity (treated as a continuous variable). This was Secondary school 309/811 38
performed while controlling for all a priori confounders including College/university 233/811 29
household wealth or maternal education, as appropriate. The statistical Treatment porridge, %
significance of the indirect effect was determined by using bias-corrected Basally fortified 406/811 50
bootstrapping to generate 95% CIs (32).
Richly fortified 405/811 50
Additional sensitivity analyses were conducted for 6- and 12-mo
dietary models controlling for current breastfeeding (i.e., breastfeeding 1
HAZ, height-for-age Z-score; WHZ, weight-for-height Z-score.
until at least 6 or 12 mo of age, respectively) and excluding those who 2
Values are means 6 SDs or percentages.

1820 Mallard et al.

 TABLE 2 Effect of baseline household wealth and maternal education on HAZ and WHZ at 18 mo1

HAZ at 18 mo WHZ at 18 mo
n or n/total n b (95% CI)2 P Adjusted b (95% CI)3 P n or n/total n b (95% CI)2 P Adjusted b (95% CI)3 P

Household wealth quintile ,0.0014 ,0.0014 ,0.0014 0.26

Lowest 120/631 Referent Referent 121/631 Referent Referent
Second 128/631 0.15 (20.03, 0.33) 0.11 0.07 (20.12, 0.25) 0.49 128/631 0.05 (20.15, 0.24) 0.65 0.09 (20.12, 0.30) 0.39
Middle 121/631 0.34 (0.15, 0.52) ,0.001 0.21 (0.02, 0.41) 0.029 121/631 0.24 (0.04, 0.44) 0.018 0.20 (20.02, 0.41) 0.07
Fourth 135/631 0.54 (0.36, 0.72) ,0.001 0.37 (0.17, 0.57) ,0.001 135/631 0.29 (0.09, 0.48) 0.004 0.22 (0.00, 0.45) 0.05
Highest 127/631 0.59 (0.41, 0.77) ,0.001 0.34 (0.13, 0.55) 0.001 126/631 0.37 (0.17, 0.56) ,0.001 0.20 (20.03, 0.45) 0.09
Maternal education ,0.0014 ,0.0014 ,0.0014 0.0144
Primary school or less 195/631 Referent Referent 196/631 Referent Referent
Secondary school 249/631 0.29 (0.16, 0.43) ,0.001 0.17 (0.02, 0.32) 0.023 249/631 0.13 (20.02, 0.28) 0.10 0.07 (20.10, 0.23) 0.42
College/university 187/631 0.60 (0.46, 0.75) ,0.001 0.43 (0.26, 0.61) ,0.001 186/631 0.33 (0.17, 0.49) ,0.001 0.25 (0.05, 0.45) 0.013
Covariates
Females 335/631 20.03 (20.15, 0.08) 0.57 20.03 (20.15, 0.9) 0.60 335/631 0.06 (20.07, 0.18) 0.37 0.10 (20.05, 0.23) 0.15
Birth weight 631 20.09 (20.23, 0.04) 0.17 20.15 (20.28, 20.01) 0.033 627 0.43 (0.31, 0.55) ,0.001 0.40 (0.27, 0.54) ,0.001
Hemoglobin 621 0.04 (20.01, 0.09) 0.13 20.02 (20.07, 0.03) 0.44 621 0.04 (20.01, 0.09) 0.16 20.02 (20.08, 0.03) 0.45
Diarrhea in past 3 mo 125/631 20.03 (20.18, 0.11) 0.67 20.02 (20.16, 0.12) 0.80 126/631 0.13 (20.02, 0.29) 0.10 0.11 (20.05, 0.27) 0.19
Infant HAZ at 6 mo 631 0.84 (0.79, 0.90) ,0.001 0.81 (0.74, 0.88) ,0.001 — — — —
Infant WHZ at 6 mo — — — — — 631 0.67 (0.61, 0.72) ,0.001 0.64 (0.58, 0.70) ,0.001
Maternal height 631 0.02 (0.01, 0.03) ,0.001 0.02 (0.01, 0.03) 0.002 631 0.02 (0.01, 0.03) 0.002 0.01 (20.01, 0.02) 0.32
HIV-exposed 149/577 20.17 (20.31, 20.03) 0.014 20.12 (20.25, 0.02) 0.09 149/577 0.01 (20.15, 0.16) 0.92 0.08 (20.07, 0.23) 0.32
Richly fortified 316/631 0.02 (20.10, 0.14) 0.73 0.06 (20.05, 0.18) 0.28 316/631 0.06 (20.06, 0.19) 0.33 0.06 (20.07, 0.18) 0.40
porridge treatment
1
HAZ, height-for-age Z-score; WHZ, weight-for-height Z-score.
2
Adjusted for baseline HAZ or WHZ only.
3
Adjusted for baseline HAZ or WHZ, household wealth and/or maternal education, sex, birth weight, baseline hemoglobin, diarrhea in last 3 mo, maternal height, HIV exposure, and treatment group.
4
P value for linear trend.

Dietary diversity predicts subsequent infant growth

1821
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fully adjusted models of WHZ, although the positive association
between maternal education and WHZ remained significant (P =
0.014 for linear trend), household wealth was rendered nonsig-
nificant (P = 0.26). No significant interaction between household
wealth and maternal education was found in models for HAZ or
WHZ at 18 mo by using either 6- or 12-mo Z-scores as
independent baseline variables (all P $ 0.15; data not shown).
WHO IYCF indicators and dietary diversity at 6 mo of age.
Although >91% of infants received MMF, only 12% and 10% of
infants received MDD and MAD, respectively, at 6 mo of age.
More than 61% of infants consumed an iron-rich/iron-fortified
food, and of all the WHO IYCF indicators this was the only
practice that was significantly related to a greater HAZ (b =
0.16; 95% CI: 0.03, 0.29; P = 0.016) and WHZ (b = 0.24; 95%
(both P # 0.004 for linear trend) (Table 3). The mean VIF of
household wealth, maternal education, and dietary diversity
score at 6 mo was low (1.27), indicating very little inflation of
the variance of estimated regression coefficients due to collin-
earity (31).
In univariate regression models with dietary diversity score as
the dependent variable, greater levels of household wealth and
maternal education were positively associated with dietary
diversity score at 6 mo (both P < 0.001 for linear trend; data not
shown). Including both household wealth and maternal educa-
tion in a multivariate model rendered household wealth
nonsignificant overall (P = 0.08), whereas the positive linear
relation between maternal education and dietary diversity
remained significant (P = 0.001 for linear trend). An interaction
term for household wealth and maternal education was not

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CI: 0.09, 0.38; P = 0.001) at 18 mo in fully adjusted analyses.
Infants consumed a median of 2 (IQR: 2–3) food groups in
the 24 h preceding the 6-mo interview. The consumption of
individual food groups was not related to HAZ at 18 mo after
adjusting for baseline variables (data not shown). The con-
sumption of food(s) containing dairy products was significantly
associated with a higher WHZ at 18 mo of age (b = 0.40; 95%
CI: 0.26, 0.55; P < 0.001), as was consumption of any animal-
source food group(s) (b = 0.41; 95% CI: 0.25, 0.56; P < 0.001).
In fully adjusted analyses, a higher dietary diversity score was
positively associated with both HAZ and WHZ at 18 mo of age
significant (P = 0.38). Dietary diversity at 6 mo was not a
significant mediator of the effect of household wealth on HAZ
and WHZ at 18 mo, after controlling for baseline anthropo-
metric measurements and a priori confounders. Conversely,
dietary diversity at 6 mo mediated 13.4% and 25.9% of the total
effect of maternal education on HAZ and WHZ, respectively, at
18 mo.
There were no meaningful differences in sensitivity analyses
controlling for current breastfeeding (i.e., breastfeeding until at
least 6 mo of age) or in those excluding infants who tested HIV
positive at 18 mo of age.

TABLE 3 WHO IYCF indicators and dietary diversity at 6 and 12 mo in relation to HAZ and WHZ at 18 mo1

6-mo dietary intakes 12-mo dietary intakes

Adjusted b Adjusted b
n (%) b (95% CI)2 P (95% CI)3 P n (%) b (95% CI)2 P (95% CI)4 P

HAZ at 18 mo5
MDD achieved6 78 (12) 0.24 (0.06, 0.41) 0.008 0.15 (20.02, 0.32) 0.08 159 (26) 0.03 (20.07, 0.12) 0.60 20.04 (20.14, 0.05) 0.36
MMF achieved6 577 (92) 0.15 (20.06, 0.37) 0.16 0.14 (20.07, 0.35) 0.20 567 (94) 0.20 (0.03, 0.38) 0.025 0.13 (20.05, 0.31) 0.16
MAD achieved6 68 (11) 0.21 (0.02, 0.40) 0.028 0.15 (20.03, 0.33) 0.11 127 (21) 0.06 (20.04, 0.17) 0.22 20.03 (20.14, 0.07) 0.54
Iron-rich foods consumed6 405 (64) 0.31 (0.19, 0.43) ,0.001 0.16 (0.03, 0.29) 0.016 410 (68) 0.07 (20.02, 0.16) 0.15 0.04 (20.07, 0.15) 0.45
Dietary diversity score ,0.0017 0.0017 0.28 0.18
#1 WHO food group 66 (11) Referent Referent 82 (14) Referent Referent
2 WHO food groups 294 (47) 0.45 (0.25, 0.64) ,0.001 0.26 (0.05, 0.47) 0.014 184 (31) 0.11 (20.02, 0.25) 0.10 0.12 (20.02, 0.26) 0.10
3 WHO food groups 190 (30) 0.53 (0.33, 0.74) ,0.001 0.33 (0.11, 0.55) 0.003 177 (29) 0.15 (0.01, 0.29) 0.030 0.14 (0.00, 0.28) 0.044
4 WHO food groups 65 (10) 0.66 (0.41, 0.91) ,0.001 0.40 (0.14, 0.66) 0.003 96 (16) 0.14 (20.01, 0.30) 0.07 0.10 (20.06, 0.26) 0.20
$5 WHO food groups 13 (2) 0.67 (0.24, 1.11) 0.003 0.48 (0.05, 0.91) 0.030 63 (10) 0.12 (20.05, 0.29) 0.17 0.01 (20.16, 0.18) 0.90
WHZ at 18 mo8
MDD achieved6 77 (12) 0.18 (20.02, 0.37) 0.07 0.13 (20.07, 0.33) 0.20 158 (26) 0.13 (0.02, 0.25) 0.019 0.10 (20.01, 0.22) 0.08
MMF achieved6 576 (92) 0.09 (20.14, 0.32) 0.43 0.19 (20.04, 0.43) 0.11 565 (94) 20.04 (20.25, 0.18) 0.73 20.08 (20.30, 0.14) 0.49
MAD achieved6 67 (11) 0.23 (0.03, 0.43) 0.026 0.18 (20.02, 0.39) 0.08 126 (21) 0.15 (0.03, 0.27) 0.018 0.13 (0.00, 0.26) 0.044
Iron-rich foods consumed6 404 (64) 0.32 (0.19, 0.45) ,0.001 0.24 (0.09, 0.38) 0.001 409 (68) 0.11 (0.00, 0.21) 0.05 0.16 (0.02, 0.30) 0.025
Dietary diversity score ,0.0017 0.0047 0.009 0.020
#1 WHO food group 67 (11) Referent Referent 82 (14) Referent Referent
2 WHO food groups 294 (47) 0.35 (0.14, 0.56) 0.001 0.28 (0.05, 0.52) 0.018 182 (30) 20.06 (20.22, 0.10) 0.48 20.10 (20.27, 0.07) 0.25
3 WHO food groups 190 (30) 0.43 (0.21, 0.65) ,0.001 0.35 (0.10, 0.59) 0.006 177 (30) 0.12 (20.04, 0.29) 0.13 0.09 (20.07, 0.27) 0.29
4 WHO food groups 64 (10) 0.44 (0.17, 0.72) 0.001 0.38 (0.08, 0.67) 0.013 95 (16) 0.16 (20.02, 0.35) 0.08 0.09 (20.11, 0.28) 0.38
$5 WHO food groups 13 (2) 0.83 (0.36, 1.30) 0.001 0.57 (0.08, 1.06) 0.023 63 (11) 0.16 (20.05, 0.36) 0.13 0.13 (20.09, 0.34) 0.25
1
HAZ, height-for-age Z-score; IYCF, infant and young child feeding; MAD, minimum acceptable diet; MDD, minimum dietary diversity; MMF, minimum meal frequency; WHZ,
weight-for-height Z-score.
2
Adjusted for HAZ or WHZ at baseline or at 12 mo of age only.
3
Adjusted for baseline HAZ or WHZ and hemoglobin, sex, birth weight, treatment group, HIV exposure, diarrhea in past 3 mo, maternal height and education, and household
wealth.
4
Adjusted for HAZ or WHZ and hemoglobin at 12 mo, sex, birth weight, treatment group, HIV exposure, diarrhea in past 6 mo, hospital admission between 6 and 12 mo, maternal
height and education, and household wealth.
5
n = 628 and 602 for 6- and 12-mo dietary intakes, respectively.
6
Referent group in all cases was not achieving variable described.
7
P value for linear trend.
8
n = 628 and 600 for 6- and 12-mo dietary intakes, respectively.

1822 Mallard et al.

WHO IYCF indicators and dietary diversity at 12 mo of age.
One-quarter (26%) of infants received MDD at 12 mo of age,
and one-fifth (21%) received MAD. Almost all (94%) of infants
received MMF, and more than two-thirds (68%) consumed an
iron-rich/iron-fortified food. In adjusted analyses, WHO IYCF
indicators at 12 mo of age were not significantly associated with
HAZ at 18 mo. Meeting the criteria for MAD and consumption
of an iron-rich/iron fortified food were positively associated with
WHZ at 18 mo [b = 0.13 (95% CI: 0.00, 0.26; P = 0.044) and
0.16 (95% CI: 0.02, 0.30; P = 0.025), respectively].
At the 12-mo interview, infants consumed a median of 3 (IQR:
2–4) food groups in the previous 24 h. In fully adjusted analyses,
the consumption of individual food groups was not related to
HAZ at 18 mo (data not shown). The consumption of food(s)
containing other fruits and vegetables or eggs was significantly
associated with a higher WHZ at 18 mo of age (both P # 0.042;
data not shown). The consumption of any animal-source food
group(s) was also significantly associated with a greater WHZ at
18 mo (b = 0.17; 95% CI: 0.06, 0.30; P = 0.003).
Dietary diversity at 12 mo was significantly associated with a
greater WHZ at 18 mo in fully adjusted analyses (P = 0.020) but
not with HAZ (Table 3). The mean VIF (1.24) indicated that there
was no problematic multicollinearity between household wealth,
maternal education, and dietary diversity score at 12 mo (31).
In univariate regression models with dietary diversity score at
12 mo as the dependent variable, greater levels of both
household wealth and maternal education were positively
associated with dietary diversity score (both P < 0.001 for linear
trend; data not shown). Including both household wealth and
maternal education in a multiple linear regression model
rendered household wealth nonsignificant overall (P = 0.27),
whereas the positive linear relation between maternal education
and dietary diversity remained significant (P = 0.001), indicating
that maternal education accounted for much of the influence of
household wealth on dietary diversity. An interaction term for
household wealth and maternal education in a multivariate
model was not significant (P = 0.87). Dietary diversity at 12 mo
was not a significant mediator of the effect of household wealth
or maternal education on WHZ at 18 mo, after controlling for
baseline anthropometric measures and a priori confounders.
Because dietary diversity at 12 mo was not associated with HAZ
at 18 mo, mediation analyses were not conducted (33).
In sensitivity analyses controlling for current breastfeeding,
iron-rich food consumption became nonsignificant in relation to
WHZ (P = 0.1). Excluding those who tested HIV positive at
18 mo of age rendered the association between MAD and iron-
rich foods at 12 mo and WHZ at 18 mo nonsignificant (both P $
0.07). Conversely, when excluding those who tested HIV
positive at 18 mo, dietary diversity at 12 mo became a significant
mediator of the effect of maternal education on WHZ at 18 mo,
mediating 17.7% of the total effect.
Discussion
In this longitudinal study of complementary food intake in a
large cohort of Zambian infants, we found that greater amounts
of dietary diversity and intake of iron-rich/iron-fortified foods at
6 mo of age were key independent predictors of subsequent
growth to 18 mo. Although a simple dietary diversity score
captured this effect, in fully adjusted analyses the WHO IYCF
binary indicator MDD did not, suggesting that it may have
misclassified diets with adequate micronutrient content as
inadequate. In the original 10-country analyses used to generate
the WHO IYCF indicators, at a cutoff of 4 food groups MDD
had a high sensitivity but low specificity for detecting diets with
inadequate micronutrient content (6). Given that the dietary
data used to produce the MDD indicator can also be used to
generate a diversity score, a score may be a superior measure of
diet quality with no additional investment in data collection
required. The precision gained by using a score rather than a
binary variable may be of particular importance in research
contexts such as ours, when regression analysis is used to
examine the complex relations between diet diversity, SEP, and
health outcomes (34).
According to the UNICEF conceptual framework, SEP-
related factors such as inadequate sanitation, lack of access to
safe water, and poor household food security are the primary
underlying causes of child malnutrition (35). Isolating the effects
of dietary diversity on child growth that operate through
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improved nutrition is difficult because dietary diversity is
associated with, and may merely reflect, SEP (19–22). In a
cross-sectional analysis of Demographic and Health Survey data
from 11 countries, dietary diversity was associated with current
infant anthropometric measurements after controlling for SEP,
as measured by maternal education and household wealth (36).
In our longitudinal study, dietary diversity at 6 mo of age was
also found to be associated with growth to 18 mo after
controlling for maternal education and household wealth,
strengthening the evidence in favor of dietary diversity as
having an influence on infant growth independent of socioeco-
nomic factors.
Unexpectedly, dietary diversity did not mediate the relation
between household food insecurity and growth status in a recent
cross-sectional analysis of baseline data from the multicountry
Alive & Thrive study on child malnutrition (37). Similarly, here
we found that dietary diversity was not a significant mediator of
the effect of household wealth on growth, suggesting that SEP-
related factors, such as level of sanitation, were responsible. In
contrast, we found that a substantial proportion of the effect of
maternal education on infant growth was mediated through the
provision of a diverse diet at 6 mo of age, while controlling for
household wealth. This demonstrates that maternal education
benefits child growth through improved complementary feeding
practices rather than solely via improved SEP. Other pathways
through which maternal education might influence child growth
besides SEP include increased autonomy and confidence in
decision making (38); improved health and nutrition knowledge,
attitudes, and practices (39); and better access to, use of, and
understanding of health information (40). Corresponding with
several previous studies (41–43), we also found that the effect of
maternal education on growth and dietary diversity superseded
that of household wealth when both variables were included in
regression modeling. Together, these findings indicate that
policies aimed at increasing the formal educational attainment
of women present a promising avenue for intervention.
Of particular interest was the finding that dietary diversity
and intake of iron-rich foods appeared to be more critical at
6 mo of age than at 12 mo of age for subsequent growth, a
finding highlighted by the rendering of several associations
between 12-mo intakes and WHZ at 18 mo as nonsignificant in
sensitivity analyses. In a prospective study in 262 HIV-exposed
infants in Ivory Coast, it was also identified that a summary
score of complementary feeding practices at 6 mo, but not at 9 or
12 mo of age, was associated with subsequent growth to 18 mo
(44). Our findings should be interpreted with caution, however,
because at 12 mo of age the infants were administered an
intervention porridge. This may have attenuated any beneficial
effect of increasing dietary diversity or intake of iron-rich foods
Dietary diversity predicts subsequent infant growth 1823
on micronutrient intakes because the porridges, particularly the
richly fortified porridge, provided additional micronutrients.
Nevertheless, the limited gastric capacity and thus high target
nutrient density requirements for infants aged 6–8 mo recom-
mended by the WHO (15) are in accordance with our findings,
and no significant difference in growth was noted between the 2
treatment groups at follow-up (23). In Zambia, as in many
countries, complementary food is commonly introduced be-
tween 4 and 6 mo of age (3), and all infants in this study had
been introduced to complementary foods before baseline at 6 mo
of age. It is likely that complementary food intake, including
nonhuman milk, partially displaces breast milk intake at this
young age (45). Hence, dietary diversity and intake of iron-rich
foods may have been more critical for ensuring adequate
micronutrient intake in our cohort than if the infants had been
exclusively breast-fed until 6 mo of age. This may have been of
particular relevance in this mixed population of HIV-exposed
and -unexposed infants because 34% of HIV-positive mothers
ceased breastfeeding completely before their infants were 6 mo
of age in accordance with contemporaneous recommendations.
Such a practice may further increase the reliance on comple-
mentary foods for the provision of micronutrients.
MMF, frequently used as an indicator of energy intake from
complementary foods, was not related to subsequent growth in
our study. However, flour for making the high-energy-density
porridge was provided to mothers in excess of the estimated
porridge consumption of the infants during the treatment period,
which may have attenuated any effect of achieving MMF at 12
mo of age on subsequent growth. In general, a lack of association
between MMF and anthropometric measures has been reported
in cross-sectional analyses across many different settings with few
exceptions (46). This observation either suggests that in most
settings energy intake from complementary foods for infants is
adequate or that adequate energy intakes alone are not sufficient
to promote infant growth (47). Complementary feeding interven-
tions may thus be more successful if focused on increasing dietary
diversity rather than the number of meals consumed. However, if
a greater number of meals also resulted in more adequate micro-
nutrient intakes through sheer quantity consumed (48), receiving
MMF may have a beneficial effect on linear growth.
We acknowledge that our analyses are based on single 24-h diet
recall interviews and are thus subject to random error resulting from
within-person variation. This may have attenuated any associations
between dietary intake and subsequent growth, although the mean
number of food groups consumed (i.e., dietary diversity) is known
to be less affected by this type of random error (48).
In conclusion, our results highlight the importance of ap-
propriate micronutrient intakes at 6 mo of age in promoting
child growth to 18 mo, as measured by a simple dietary diversity
score calculated by using the WHO-defined food groups and the
WHO IYCF indicator for iron-rich foods. Interventions to
increase infantsÕ dietary diversity and iron-rich food intake
should thus be targeted toward this early period of complemen-
tary food introduction when nutrient needs are greatest. An
equally important finding was that the influence of maternal
education on child growth lies in part with the diversity of food
provided to the child. In addition to the implementation of
policies to increase the level of formal education among women,
IYCF education programs should be targeted toward women
with little formal education, because higher maternal nutrition
knowledge has been demonstrated to partially compensate for
low education in some contexts (39,49). Although it was not
evident from our middle-income study setting, it should be noted
that the beneficial influence of maternal knowledge or formal
1824 Mallard et al.
education on child growth is understood to be dependent on a
minimum level of access to resources (39,50–53). Nonetheless,
our findings support the growing interest in increasing maternal
educational attainment as a potential intervention toward im-
proving child health outcomes (18,54–56).
Acknowledgments
The authors thank Andrew Gray, Senior Research Fellow in
Biostatistics, Department of Preventive and Social Medicine,
University of Otago, for his statistical advice for the current
analyses and Kathy Baisley, Lecturer in Epidemiology and
Medical Statistics, Department of Infectious Disease Epidemi-
ology, London School of Hygiene and Tropical Medicine, for
her previous statistical work on the CIGNIS trial. S.F. and R.S.G.
designed and conducted the original CIGNIS trial; M.C. and J.S.
Downloaded from https://academic.oup.com/jn/article-abstract/144/11/1818/4590073 by guest on 13 October 2019
managed the CIGNIS trial and collected data; A.M. and J.N.
collected and/or checked the dietary data; S.R.M., L.A.H., and
R.S.G. conceived the idea for the current study; and S.R.M.
cleaned and analyzed the data, wrote the manuscript, and had
primary responsibility for its final content. All authors read and
approved the final version of the manuscript.
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Dietary diversity predicts subsequent infant growth 1825