Received: 8 June 2017 Revised: 10 November 2017 Accepted: 27 November 2017

DOI: 10.1111/mcn.12584

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ORIGINAL ARTICLE

Early childhood growth and cognitive outcomes: Findings from

the MAL‐ED study*
Rebecca J. Scharf1,2 | Elizabeth T. Rogawski2,14 | Laura E. Murray‐Kolb3 |

Angelina Maphula4 | Erling Svensen5 | Fahmida Tofail6 | Muneera Rasheed7 |

Claudia Abreu8 | Angel Orbe Vasquez9 | Rita Shrestha10 | Laura Pendergast11 |

Estomih Mduma12 |
Beena Mark R. Koshy13 | Conaway14 | James A. Platts‐Mills2 |
2 |
Richard L. Guerrant Mark D. DeBoer1

1
Department of Pediatrics, University of
Virginia, Charlottesville, Virginia, USA Abstract
2
Center for Global Health, Department of Although many studies around the world hope to measure or improve developmental progress in
Medicine, University of Virginia, children to promote community flourishing and productivity, growth is sometimes used as a
Charlottesville, Virginia, USA surrogate because cognitive skills are more difficult to measure. Our objective was to assess how
3
Department of Nutrition Sciences, Penn childhood measures of anthropometry correlate with measures of child development in low‐
State University, University Park,
income settings with high prevalence of poor nutrition and enteric disease, to inform studies
Pennsylvania, USA
4 considering growth outcomes in the absence of direct child developmental skill assessment.
Department of Psychology, University of
Venda, Thohoyandou, South Africa Children from the MAL‐ED study were followed from birth to 24 months of age in field sites in 8
5
Department of Global Health and Primary low‐ and middle‐income countries across 3 continents. Monthly weight, length, and head
Care, University of Bergen, Bergen, Norway circumference measurements were performed. At 24 months, the Bayley Scales of Infant and
6
Center for Nutrition and Food Security, Toddler Development was administered. We correlated cognitive measures at 24 months with
icddr‐b, Dhaka, Bangladesh
anthropometric measurements from birth to 2 years comparing 3 constructs: absolute attained
7
Department of Paediatrics and Child Health,
monthly measures, summative difference in measures from the mean growth curve, and rate
Aga Khan University, Karachi, Pakistan
8 of change in measures. Growth faltering at multiple time periods is related to Bayley cognitive
Department of Microbiology, Federal
University of Ceará, Fortaleza, Brazil outcomes at 24 months. Birthweight, overall growth by 18–24 months, and rate of growth in the
9
Department of Psychology, PRISMA, Iquitos, 6‐ to 18‐month period were most associated with 24‐month developmental scores. In this study,
Peru head circumference measurements, compared with length, was more closely linked to cognitive
10
Department of Psychology, Siddhi Memorial scores at 24 months. Notably, all studies between growth and cognitive outcomes exhibited low
Hospital, Bhaktapur, Nepal
r2 values (0.001–0.049). Anthropometric measures, particularly head circumference, were related
11
Department of Psychology, Temple
to cognitive development, although explaining a low percent of variance. When feasible, direct
University, Philadelphia, Pennsylvania, USA
12
measures of child development may be more useful.
Haydom Global Health Research Centre,
Haydom, Tanzania
13 KEY W ORDS
Department of Developmental Pediatrics,
Christian Medical College, Vellore, India early childhood development, stunting, malnutrition, growth, global health, cognition
14
Department of Public Health Sciences,
University of Virginia, Charlottesville, Virginia,
USA

Correspondence
Rebecca J. Scharf, Division of Developmental
and Behavioral Pediatrics, University of

*
see MAL‐ED‐Network‐Investigators (2014), complete list of MAL‐ED investigators are listed in the Appendix section.
The Etiology, Risk Factors and Interactions of Enteric Infections and Malnutrition and the Consequences for Child Health and Development Project (MAL‐ED) is carried
out as a collaborative project supported by the Bill & Melinda Gates Foundation, the Foundation for the NIH, and the National Institutes of Health, Fogarty Interna-
tional Center.

Matern Child Nutr. 2018;14:e12584. wileyonlinelibrary.com/journal/mcn © 2018 John Wiley & Sons Ltd 1 of 11
https://doi.org/10.1111/mcn.12584
2 of 11 bs_bs_banner
SCHARF ET AL.

Virginia School of Medicine, PO Box 800828,

Charlottesville, VA 22908, USA.
Email: rebeccascharf@virginia.edu
Funding information
Bill & Melinda Gates Foundation, Grant/Award
Number: OPP47075; Doris Duke Charitable
Foundation (RJS), Grant/Award Number:
CSDA 17677

1 | I N T RO D U CT I O N
Key messages
Growth faltering in young children is a challenge worldwide in settings
of undernutrition and enteric disease. Children not meeting their • Stunting has been associated with cognitive delay in
growth potential may not be meeting their developmental potential smaller studies around the world.
either, leading to diminished flourishing of societies. Poor linear • Stunting has sometimes been used as a proxy for
growth, or stunting (height‐for‐age z‐score < −2), may follow child- estimating global rates of cognitive development in
hood enteric disease or undernutrition (R. E. Black, Victora, et al., children.
2013; Checkley et al., 2008; Guerrant, Oria, Moore, Oria, & Lima, • This analysis of three growth parameters (length, weight,
2008; Lu, Black, & Richter, 2016; Prendergast & Humphrey, 2014), and head circumference) in early life in a large, recent
and some studies around the world have estimated rates of cognitive international birth cohort found that physical growth in
development and productivity based upon levels of stunting (R. E. Black, early life was related to cognitive development at age 2.
Alderman, et al., 2013; Bornstein et al., 2012; Grantham‐McGregor
• In particular, head circumference was most correlated
et al., 2007). Many studies in global health settings are interested
with 2‐year‐old Bayley cognitive scores. However,
in child development as an outcome but use height attainment as a
variance explained was low, and direct measures of
proxy outcome (Bhutta et al., 2013; Dewey & Adu‐Afarwuah,
child development add important information.
2008; Humphrey et al., 2015; Prendergast & Humphrey, 2014).
Anthropometry has been used as a surrogate for cognitive develop-
ment, as cognitive development is harder to measure and is better
measured at older ages. For example, worldwide estimates of chil-
dren not meeting their developmental potential have been based be examined at certain time points (e.g., monthly measurements) to
on stunting rates along with poverty indicators (Bornstein et al., determine if measurements from specific time points are most related
2012; Grantham‐McGregor et al., 2007; Subramanian, Ozaltin, & to developmental progress (Borghi et al., 2006). Third, it may be useful
Finlay, 2011). Although growth has previously been related to devel- to examine, taking into account the starting point and rate at which a
opmental skills in smaller studies around the world (Chang, Walker, child grows, the summative growth achieved; overall size may take
Grantham‐McGregor, & Powell, 2002; Gandhi et al., 2011; Guerrant, into account growth patterns along the way and present a summary
Deboer, Moore, Scharf, & Lima, 2013; Tarleton et al., 2006), more of the time period (de Onis et al., 2004). Finally, studying rate of
information is needed about relationships between growth and growth may be useful (Sansavini et al., 2014; Zhang, McArdle, &
development. Nesselroade, 2012). Children may have an acceleration or decelera-
Measuring early growth monitors health and development (de Onis tion in growth rate, or may follow along a growth curve (z‐score) con-
et al., 2012), and several early anthropometry measurements—weight sistently, which may have particular relationships to their brain
(de Onis, Blossner, Borghi, Morris, & Frongillo, 2004), length (Berkman, development.
Lescano, Gilman, Lopez, & Black, 2002; Prendergast & Humphrey, Because post‐natal growth has been routinely and is frequently
2014), and head circumference (Ivanovic et al., 2004; Miller et al., collected around the world as an outcome in studies of enteric dis-
2016)—carry particular implications for maturation (American Academy ease, we used data from a large, global cohort of children from
of Pediatrics, 2015). Children in settings of undernutrition and enteric research study sites to examine how growth faltering from birth to
disease are at risk for insufficient brain growth, as well as linear growth. 24 months is related to cognitive outcomes measured by the Bayley
One commonly used marker of brain growth is head circumference Scales of Infant and Toddler Development (Bayley, 2006). Our goal
(Eichorn & Bayley, 1962; Wright & Emond, 2015), particularly in the was to evaluate measures of growth as predictors of cognitive devel-
first year of life when growth is most rapid before the fontanelles are opment at 24 months using three growth parameters (length, weight,
closed and skull sutures fuse (Alamo‐Junquera et al., 2014; Scharf, and head circumference) and four constructs for evaluating growth
Stroustrup, Conaway, & DeBoer, 2015). Early growth has implications (birthweight, individual measures at specific time points, summative
for adult health (Barker, 2006; DeBoer et al., 2012). Birthweight is growth, and rate of growth). We sought not to examine all proximal
one measure of a child's endowment from the prenatal period; this determinants of development, but instead to determine which compo-
may be reflective of maternal nutrition, illness, or stress and genetic nents of growth best correlate, to inform future studies considering
factors influencing fetal development (Binkin, Yip, Fleshood, & anthropometric outcomes when direct cognitive assessment is not
Trowbridge, 1988; Patrick et al., 2005). Next, growth estimates can possible.
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2 | METHODS original item (Murray‐Kolb et al., 2014). Psychometric analyses were

completed, and items with sufficient variability were kept (range 0–15).
All measures had quality checks in place. Upon examination of
2.1 | Setting and participants
videos of assessments, it was determined that the Bayley assess-
Data collection for The Etiology, Risk Factors, and Interactions of ments were not administered with sufficient uniformity in our Tanza-
Enteric Infections and Malnutrition and the Consequences for Child nia site to allow the use of the data; following psychometric analyses,
Health (MAL‐ED) study took place in approximately 200 children from the cognitive Bayley data from Nepal were excluded because
each field site in areas of malnutrition and enteric disease in eight low‐ answers to questions performed differently in this population com-
and middle‐income countries: Bangladesh (Dhaka, urban), Brazil pared with the other six; thus, these sites were not included in
(Fortaleza, urban), India (Vellore, urban), Nepal (Bhaktapur, urban), Peru analyses. Upon analysis of growth data for quality, head circumfer-
(Loreto, rural), Pakistan (Naushahro Feroze, rural), South Africa (Venda, ence data from our Pakistan and Brazil sites and length from our
rural), and Tanzania (Haydom, rural). Institutional Review Boards for Pakistan site were not found to have sufficient quality and thus were
each site and associated universities approved the study protocol. excluded.
Clinical Trial Registration was NCT02441426. Specifics about each
study site, including the participant characteristics, can be found
elsewhere (MAL‐ED Network Investigators, 2014). Children born
2.4 | Analysis
<1,500 g, who had serious illness or extended hospital stays, multiple
gestations, and whose mothers were <16 years, were excluded. Growth measurements were converted into weight‐for‐age, length‐for‐
age, and head‐circumference‐for‐age z‐scores (WAZ, LAZ, and HCZ,
respectively) using the WHO growth curves (de Onis et al., 2012). When
2.2 | Anthropometry using weight‐for‐length z‐scores as the outcomes, results were overall
consistent with results using WAZ, although WAZ was generally more
Each month, trained field workers went to the home and recorded
strongly associated with 24‐month cognitive score (data not shown).
measurements of weight, length, and head circumference from study
We assessed four growth constructs based on monthly measure-
enrolment (mean: 7 days, range 0–17 days) to 24 months. Measure-
ments of weight, length, and head circumference (Figure S1):
ments were collected according to a standardized procedure across
all sites. Weight was measured on a digital scale calibrated weekly
using standard weights. Infants were naked or in a clean, dry diapers 1. Initial size: Cross‐sectional WAZ at enrolment within 17 days of

and weighed to the nearest 10 g (0.01 kg). Scales (Seca 354 or Detecto birth (proxy for birthweight).

8440) were calibrated weekly using standard weights. Length was 2. Attained size: WAZ, LAZ, and HCZ at monthly cross sections from
measured using a measuring board. Length was measured using a 0 to 2 years.
measuring board (Seca 417, ShorrBoard, UNICEF 0114500, or Seca 3. Summative growth: Area between child's growth curve and the
217). Hair clips, socks, and shoes were removed, and two field workers WHO growth curve; areas calculated from birth to 24 months
recorded the lengths to the nearest 0.1 cm. Head circumference was and in 6‐month intervals as
measured using nonstretch Teflon measuring tape (Seca 212) by
positioning the tape just above the eyebrows, above the ears, and 24
∑ ðWAZ i −WAZi−1 Þ*ðti −ti−1 Þ;
around the biggest part of the back of the head to the nearest 0.1 cm. i¼0

where i is an index of monthly measurements from 0 to 24 months and

2.3 | Cognitive t is age in months. Positive areas indicate growth above, whereas
The Bayley Scales of Infant and Toddler Development III (Bayley) negative areas indicate growth below the WHO mean.
were chosen to assess global child development at 24 months in the
MAL‐ED study (Bayley, 2006; Murray‐Kolb et al., 2014). The assess- 4. Growth rate: ΔWAZ/Δt, ΔLAZ/Δt, and ΔHCZ/Δt where Δt was
ment took 45–60 min and was conducted in a location that was quiet time from birth to 24 months in 6‐month intervals (0–6, 6–12,
and comfortable, with few distractions. The Bayley has been shown to 12–18, and 18–24 months). Rates were calculated by using the
be a sensitive measurement of child development; infant performance estimated slope coefficient from a fitted linear regression to the
on the tasks in the cognitive assessment has been shown to correlate anthropometry measurements over each 6‐month period taking
with later cognitive abilities (Fagan & McGrath, 1981). into account each monthly measurement; this allowed equal
Several of the MAL‐ED sites had used the Bayley in previous contribution from all measures in the time window and missing
studies, and it is a widely used assessment of child development world- growth measurements.
wide. In order to use the Bayley, we translated, adapted, and piloted the
assessment for each research site. Each assessment was translated from When children were missing a single monthly measurement, the
English to the local language(s) and then back translated by a separate average of the prior and following months was used as the missing
researcher to ensure accurate translation. Items needing cultural trans- measurement. Attained size indicates the outcome of the growth
lation were adapted to local culture and then piloted on a separate process and does not take into account the shape of the trajectory.
group of children to ensure comparable difficulty of each item to the Conversely, growth rate describes the rapidity of growth but does
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not consider where the child falls in relation to the average growth anthropometry and Bayley scores measured at 24 months. Participants
curve. A high growth rate may indicate strong growth in well‐ without 24‐month Bayley scores (compared to those with 24‐month
nourished children as well as catch‐up growth among malnourished Bayley measures) had similar gender proportions (51% male vs. 48%
children. Cumulative growth combines both the magnitude and rate male, χ2 p value = .11) but were more likely to be from rural settings
components of growth. Because each construct is calculated with (52% vs. 46%, χ2 p value = .02) and had higher enrolment weight
different units, we standardized the growth constructs into sample‐ (3.19 kg vs. 3.07 kg, t test p value < .0001). Enrolment weights (taken
Xi −μ in the first 2 weeks of life) of the study sample had a mean of
based z‐scores ( zi ¼ , where Xi is the child's growth construct
σ 3.07 kg and ranged by research site, from a mean of 2.77 kg in the
value, μ is the total sample mean of the growth construct, and σ is
Bangladesh research site to 3.48 kg in the Brazil site. Ninety‐seven
the standard deviation of the growth construct) to compare effect
percent of children in the analysis had birthweights in the WHO
sizes across constructs.
normal range (2,000–5,000 g) at study start (Figure S2). Over the 2‐
We used multivariable linear regression to estimate the associa-
year study period, there was variation among the research sites with
tion between each construct of WAZ, LAZ, and HCZ with separate
regards to height, weight, and head circumference achieved; for
regression models at different ages with cognitive outcome at
example, head circumference z‐scores ranged from −2.01 in the India
24 months, adjusting for research site and enrolment weight.
site to 0.20 in the South Africa site.
These analyses were completed to specifically examine the non-
causal association between anthropometry and early childhood devel-
opment to assess the ability of anthropometry to serve as convenient 3.2 | Enrolment weight and child development
and field‐ready proxy for child development by 24 months where col- We first evaluated enrolment weight as a predictor of the cognitive
lection is limited to anthropometric observations, for example, cross‐ subscale at 24 months. Figure 1 shows the adjusted mean Bayley
sectional survey data. Therefore, other potential contributors to cogni- cognitive score for each enrolment WAZ category, adjusted for study
tive outcomes in children (socio‐economic status, early language expo- site. Children born with a birthweight z‐score more than two standard
sure, developmental stimulation, parental education or income, play deviations below the mean had the lowest Bayley scores at
opportunities, poor diet, poverty, infection, etc.) were not included as 24 months.
covariates in the present analysis, but analyses were examined and
commented upon in Section 4.
3.3 | Monthly anthropometry measures and
cognitive development
3 | RESULTS
When assessing the associations between anthropometry measure-
ments taken at each month separately with Bayley scores, adjusting
3.1 | Cohort characteristics for birthweight and research site, we found that the score on the
We examined data from 1,210 children across eight research sites in cognitive subtest was significantly related to weight, length, and head
the MAL‐ED study. There was wide variation in achieved growth circumference measurements. The regression analysis estimates for
between the sites (Table 1). Out of 1,887 newborn infants who had each measurement are plotted by month as related to cognition in
enrolment weights to be included in the study and were eligible for Figure 2. Overall, the growth constructs in the second year of life were
analysis, we examined data from 1,210 children who had both more positively correlated with cognitive scores than constructs in the

TABLE 1 Sample population, enrolment weight, and 24‐month anthropometry z‐scores for each research site
Enrolment Enrolment Enrolment 24‐month 24‐month 24‐month
Research sitea N % female weight (kg) length (cm) HC (cm) LAZ WAZ HCZ

All 1210c 48.7 3.07 ± 0.51 49.2 + 2.2 34.2 + 1.6 −1.56 ± 1.14 −1.05 ± 1.17 −1.04 ± 1.23
Bangladesh (Dhaka) 188 50.5 2.77 ± 0.40 48.3 + 2.0 33.6 + 1.4 −2.04 ± 0.95 −1.63 ± 0.97 −1.87 ± 0.96
Brazil (Fortaleza) 140 42.1 3.48 ± 0.53 49.8 + 2.1 35.2 + 1.4 −0.02 ± 1.10 0.34 ± 1.22 NAb
India (Vellore) 227 53.7 2.93 ± 0.46 49.3 + 2.1 33.4 + 1.3 −1.92 ± 0.97 −1.65 ± 0.94 −2.01 ± 0.78
Nepal (Bhaktapur)d 224 46.4 3.15 ± 0.46 50.1 + 2.1 34.2 + 1.2 −1.34 ± 0.92 −0.93 ± 0.90 −0.95 ± 0.88
Peru (Loreto) 197 45.7 3.08 ± 0.44 48.6 + 1.9 33.7 + 1.4 −1.89 ± 0.87 −0.79 ± 0.91 −0.58 ± 0.96
Pakistan (Naushahro Feroze) 245 50.6 2.90 ± 0.49 48.7 + 2.4 33.9 + 1.5 NA −1.65 ± 0.99 NA
South Africa (Venda) 213 48.8 3.31 ± 0.47 49.6 ± 1.9 35.5 + 1.3 −1.71 ± 1.04 −0.51 ± 0.98 0.20 ± 1.02
Tanzania (Haydom)d 254 51.3 3.38 ± 0.47 48.9 + 2.4 35.1 + 1.4 −2.67 ± 1.02 −1.33 ± 1.01 −0.77 ± 0.98

Note. HC = head circumference; LAZ = length‐for‐age z‐score; WAZ = weight‐for‐age z‐score; HCZ = head‐circumference‐for‐age z‐score.
a
Data represented as mean ± SD.
b
NA: Data not of sufficient quality to include in the study.
c
Total N used in the analyses (children with anthropometry and Bayley scores to 24 months) excludes participants from the Tanzania and Nepal sites as the
Bayley data were not collected with sufficient reliability to be included in the analyses.
d
Bayley cognitive data not included in analyses.
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(a) WAZ
0.75

1 z-score increase in WAZ

cognitive score per
Change in 24-mo
0.50

0.25

0.00

-0.25

-0.50 6 12 18 24
Age (months)
(b)
0.75 LAZ

1 z-score increase in LAZ

cognitive score per
Change in 24-mo
0.50

0.25
FIGURE 1 Mean 24‐month Bayley cognitive score by category of
enrolment weight z‐score (adjusted by site). Overall model linear 0.00
trend test p = 0.02
-0.25

-0.50 6 12 18 24
first year of life. Of note, head circumference was more strongly
Age (months)
associated with cognitive skills than LAZ or WAZ; for an average
increase of 1 HCZ, Bayley cognitive score (range of 0 to 15) increased (c) HCZ
0.75
1 z-score increase in HCZ

0.37 points.
cognitive score per
Change in 24-mo

0.50
3.4 Summative anthropometry measures and child
|
0.25
development
0.00
We next assessed how summative growth area from the growth curve
was related to Bayley cognitive scores (Figure 3). Summative linear -0.25
growth was not linked to 24‐month Bayley scores at any of the time
intervals, whereas summative weight area was only significantly -0.50 6 12 18 24
associated with 24‐month Bayley scores from 18 to 24 months. Age (months)
Summative head circumference from 12 to 18 and 18 to 24 months FIGURE 2 Associations between attained growth z‐scores from 1 to
was significantly related to cognitive skills. Therefore, taking into 24 months of age with Bayley Cognitive Score at 24 months of age.
account summative growth over time, head circumference was again Mean difference (95% confidence interval) in cognitive score at
a stronger predictor of cognitive scores than weight and length and 24 months associated with an increase in attained growth z‐score by 1
at each month (analysed in separate regressions) from 1 to 24. (a)
later total growth (the 18‐ to 24‐month period in particular) was most
Weight‐for‐age z‐score (WAZ). (b) Length‐for‐age z‐score (LAZ). (c)
closely linked (Figure 3). Head‐circumference‐for‐age z‐score (HCZ). Regressions are adjusted
for research site and enrolment weight

3.5 | Rate of growth and child development weight, length, or head circumference [assessed separately] vs.
Finally, we examined slope, or rate of growth, over time. Growth others). Children born in low anthropometry categories did not
rates over 6‐month periods were most related to Bayley cognitive exhibit significantly different relationship between rate of growth
score between 6 and 18 months (Figure 4). Growth rate in length and 24‐month Bayley scores.
6 to 12 months, and head circumference 6 to 12 and 12 to Our analyses focused on whether measures of childhood anthro-
18 months were positively related to cognitive scores. Rapid rate pometry were associated with later measures of Bayley scores of
of change for weight, length, and especially head circumference at cognition. However, in a separate sensitivity analysis, we assessed
18 to 24 months was related to lower scores. As a sensitivity anal- whether these measures remained associated after adjusting for
ysis, we assessed whether the relationship between growth rate the presence of confounding factors, including maternal reasoning
(slope) and Bayley score differed when participants were stratified abilities (score on the Raven Combined Progressive Matrices),
by enrolment anthropometry measure category (i.e., children who maternal education (years of schooling), and child stimulation (score
were smaller than two standard deviations below the mean for on Home Observation of the Measured Environment). Inclusion of
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SCHARF ET AL.

(a) WAZ Area on Cognitive (a)

WAZ Slope
increase in summative WAZ

score per 1 z-score increase in

Change in 24-mo cognitive
1.0

WAZ slope per time interval

1.0

Change in 24-mo cognitive

score per 1 z-score

0.5
0.5

0.0

0.0
-0.5

-0.5 -1.0
6

12

18

24

12

4
6
0-

0-

-1

-2
6-

-
12

18

6-

12

18
Time window Time window
(months) (months)
(b)
(b) LAZ Area on Cognitive LAZ Slope

score per 1 z-score increase in

LAZ slope per time interval
1.0
increase in summative LAZ

Change in 24-mo cognitive

Change in 24-mo cognitive

1.0
score per 1 z-score

0.5
0.5
0.0

0.0 -0.5

-1.0
-0.5

12

4
6
0-

-1

-2
24
12
6

18

6-
0-

12

18
-

-
6-

18
12

Time window
Time window (months)
(months) (c)
HCZ Slope
score per 1 z-score increase in

(c) HCZ Area on Cognitive

HCZ slope per time interval

1.0
Change in 24-mo cognitive
increase in summative HCZ
Change in 24-mo cognitive

1.0
0.5
score per 1 z-score

0.5 0.0

-0.5
0.0
-1.0
12

4
6

-0.5
0-

-1

-2
6-

12

18
6

12

4
-1

-2
0-

6-

Time window
12

18

Time window (months)

(months) FIGURE 4 Mean difference (95% confidence interval) in cognitive
FIGURE 3 Mean difference (95% confidence interval) in cognitive score at 24 months associated with an increase in growth rate z‐
score at 24 months associated with an increase in summative growth score by 1 for 6‐month intervals between 0 and 24 months. (a)
z‐score by 1 for 6‐month intervals between 0 and 24 months. (a) Weight‐for‐age z‐score (WAZ); (b) Length‐for‐age z‐score (LAZ); (c)
Weight‐for‐age z‐score (WAZ). (b) Length‐for‐age z‐score (LAZ). (c) Head‐circumference‐for‐age z‐score (HCZ)
Head‐circumference‐for‐age z‐score (HCZ)

these factors was generally significantly linked to 24‐month Bayley

3.6 | R2 values from regression analyses
and did diminish the magnitude of the association with the Table S1 provides r2 values for the anthropometric assessment from
anthropometric measures in some cases but importantly did not alter each of the above regression analyses, without research site or enrol-
the direction or significance of association of the anthropometry ment weight in the models. Values were low, including from analyses
measures (data not shown). with significant associations.
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4 | DISCUSSION window, possibly representing concerns such as hydrocephalus,

genetic disorders, or other medical challenges.
Anthropometric measures in the first 2 years of life were associated Although measuring cognitive development directly provides the
with developmental score at 2 years of age in this multisite study of most developmental information, population studies continuing to
children in settings of malnutrition and enteric disease on three use linear growth as a surrogate for developmental potential due to
continents. Birth size, rate of growth in the 6‐ to 18‐month period, resource constraints may find it useful to include head circumference,
and overall growth by 18–24 months of age were most associated with in addition to height. Brain growth has important implications for
24‐month cognitive scores. This suggests that early childhood growth cognitive development (Grantham‐McGregor et al., 2007). Children
is indeed related to developmental skills and may be a reasonable who are not adequately nourished or who experience chronic illness
surrogate for cognition in clinical studies, when there are difficulties may not have adequate nutrients to promote brain growth, formation
in assessing developmental outcomes directly. of continued neural connections, and myelination of nerve pathways
in the critical first 3 years of brain development (Cornelio‐Nieto,
2007; Georgieff, 2007; Shonkoff, 2011; Shonkoff & Phillips, 2000;
4.1 | Weight, length, and head circumference Thompson & Nelson, 2001). Chronic illness and poor nutrient intake
We assessed anthropometry using multiple approaches, reflecting influence early brain development (Georgieff, 2007) in the first 1,000
different aspects of childhood growth and its timing. Individual anthro- days from conception until toddlerhood (Chin‐Lun Hung et al., 2015;
pometric measures varied in their strength of association with child Streimish et al., 2012). Early neurodevelopment has significant
cognition. In this cohort of children from developing areas, head impact on learning (Belfort et al., 2011; M. M. Black et al., 2016;
circumference was perhaps the most robust predictor of development Daelmans et al., 2016; Grantham‐McGregor et al., 2007). Head circum-
at 24 months, demonstrated by consistent correlations with cognitive ference is not routinely measured in national surveys but could provide
outcomes over extended time periods—particularly 9–24 months. additional information with respect to child health and development.
Length, possibly the most commonly used outcome in studies (Bhutta In this analysis, length, weight, and head circumference were
et al., 2013; Dewey & Adu‐Afarwuah, 2008; Prendergast & Humphrey, associated with cognitive outcomes at 24 months, even when
2014), because it is less susceptible than weight to short‐term fluctua- adjusting for birthweight. This demonstrates that after controlling for
tions, was less associated with cognitive outcomes, with monthly birth endowment, post‐natal growth was related to developmental
associations that were only statistically significant at 16, 17, and outcomes. Birthweight was also related to developmental outcomes;
19 months. After 15 months, weight was positively associated with both prenatal and post‐natal influences contribute to growth, learning,
cognitive outcomes. In comparing the different ways to analyse and development.
growth, we found that rate of growth (slope) was similar in strength We noted low r2 values for these relationships between anthro-
to the individual monthly measures or summative growth (area). pometry and cognition, even in analyses with significant associations,
In comparing the different analytic approaches, we found that rate suggesting that these models do not explain much of the variability
of growth was not as strong of a predictor of later child development in cognitive scores. While outside the scope of this current analysis,
compared to individual monthly measures or summative growth. other factors (such as parental reasoning ability and educational level)
Indeed, although larger size between 18 and 24 months was associated likely predominate as predictors. The magnitude of the association
with higher cognitive scores, children still growing at a rapid rate was small, for example, a one standard deviation change in any anthro-
(potentially “catch‐up” growth) between 18 and 24 months were more pometric z‐score only predicted a difference in the Bayley Cognitive
likely to have lower cognitive scores. This is reflected in the difference score of approximately 0.5 points, which is 3% of the total scale,
in the pattern of these associations between Figures 3 and 4. It is ranging from 0 to 15 points. Therefore, direct measures of child devel-
notable that the monthly attained growth measures were just as opment around the world will add useful information beyond reliance
associated with cognitive score as the more complicated rate or on growth measurements alone if at all possible.
summative measures, which is reassuring because they are frequently The MAL‐ED study allows for comprehensive, recent data in
employed in studies following growth as a proxy for cognition (Dewey children from eight research sites on three continents to be examined
& Adu‐Afarwuah, 2008; Humphrey et al., 2015). in detail. It is rare for consistent developmental assessments to be used
Compared to earlier or later intervals, the rate of growth from 6 to in so many research sites worldwide. The cognitive subcommittee of
18 months was most tightly associated with 24‐month cognitive the MAL‐ED study team ensured a uniform protocol across all study
scores. This corresponds to a time when children are exposed to an sites, and that the assessment was translated and adapted in ways that
increasing variety of complementary foods and thus are at greater risk were comparable to the original assessment. The strengths of the
of exposure to pathogens (de Onis et al., 2004, Tarleton et al., 2006, study include careful, monthly anthropometry measurements on a
R. E. Black, Victora, et al., 2013, Platts‐Mills et al., 2015). The rate of large birth cohort of children and a comprehensive child development
growth of head circumference was a positive predictor in this period, team with a representative from each study site. Nevertheless, limita-
but it was a negative predictor from 18 to 24 months. This is likely tions include the potential for cultural differences in assessment of
explained by the fact that after the time period where the fontanelles developmental skills. In addition, Bayley data from two of the eight
are usually closed (12–18 months; American Academy of Pediatrics, research sites, head circumference from two sites, and length from
2015; Eichorn & Bayley, 1962), rapid head growth may be a negative one site were of insufficient quality to be included in these analyses,
sign, indicating that the fontanelles may not have fused in the typical potentially altering results. We also lacked information regarding
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SCHARF ET AL.

gestational age. However, children who required prolonged hospitali- the cognitive assessments for the Naushahro Feroze, Pakistan, research
zation after birth or were born <1,500 g were excluded from the study. site. BK oversaw the cognitive assessments for the Vellore, India,
A total of >97% of participants were in the normal range for research site. RS oversaw the cognitive assessments for the Bhaktapur,
birthweight by WHO; thus, it does not appear that a significant Nepal, research site. AOV oversaw the cognitive assessments for the
number of these children were born prematurely. Iquitos, Peru, research site. MRC gave input to the analyses, helped to
Following developmental skills longer than 24 months will be run the analyses, and gave critical feedback to the manuscript. LEMK
informative as later assessments have better established correlations and LP give leadership to the cognitive committee for the MAL‐ED
with adult metrics; growth and developmental assessment data until study, conceptualized the analyses, and gave critical input. RLG
age 5 are currently being collected and will be the subject of future contributed to the conceptual framework, critically read, and revised
analyses. Our study team is gathering data on cognitive, language, the manuscript. All authors critically read and approved the manuscript.
and executive function skills in these children at age 5 and examining
the many predictors of school readiness skills, including growth. ORCID
Children grow most quickly in the first 3 years of life and thus may Rebecca J. Scharf http://orcid.org/0000-0002-3381-5594
be the most vulnerable to influences, both positive and negative, on
growth as well as brain development and cognition. These data may RE FE RE NC ES
have relevance for the planning and interpretation of studies with a Alamo‐Junquera, D., Sunyer, J., Iniguez, C., Ballester, F., Garcia‐Esteban, R.,
goal of assessing or improving childhood potential. This highlights the Forns, J., … Julvez, J. (2014). Prenatal head growth and child neuropsy-
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critical nature of early childhood and the importance of promoting
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health in order to foster growth and development (Chan, Lake, &
American Academy of Pediatrics (2015) Bright futures: Prevention and
Hansen, 2016; Lo, Das, & Horton, 2016). health promotion for infants, children, adolescents, and their families.
The first 2 years of life represent tremendous growth, both In: Bright futures. (ed American Academy of Pediatrics). American
physically and cognitively. We found that measurements of head Academy of Pediatrics, Elk Grove, IL.

circumference were most predictive of cognitive scores at age 2. Barker, D. J. P. (2006). Adult consequences of fetal growth restriction.
Clinical Obstetrics and Gynecology, 49, 270–283.
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(a) direct measures of developmental progress because measures of Antonio, TX: The Psychological Corporation.
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child health and development and identify those children who may the Maternal and Child Nutrition Study Group. (2013). Evidence‐based
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The authors thank the families and children, as well as the staff, of the Lu, C., … Lancet Early Childhood Development Series Steering
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and Drs. Crystal Patil, Ben McCormick, and Laura Caulfield for critical Black, R. E., Alderman, H., Bhutta, Z. A., Gillespie, S., Haddad, L., Horton, S.,
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nutrition: Building momentum for impact. Lancet, 382, 372–375.

CONF LICT S OF INT ER E ST Black, R. E., Victora, C. G., Walker, S. P., Bhutta, Z. A., Christian, P., de Onis,
M., … Maternal and Child Nutrition Study Group. (2013). Maternal and
The authors declare that they have no conflicts of interest. child undernutrition and overweight in low‐income and middle‐income
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SUPPORTING I NFORMATION
Carreon, Danny: FIC, NIH, Bethesda, MD, USA;
Additional Supporting Information may be found online in the
Charu, Vivek: FIC, NIH, Bethesda, MD, USA;
supporting information tab for this article.
Dabo, Leyfou: FIC, NIH, Bethesda, MD, USA;
Doan, Viyada: FIC, NIH, Bethesda, MD, USA;
Graham, Jhanelle: FIC, NIH, Bethesda, MD, USA;
How to cite this article: Scharf RJ, Rogawski ET, Murray‐Kolb Hoest, Christel: FIC, NIH, Bethesda, MD, USA;
LE, et al. Early childhood growth and cognitive outcomes: Find- Knobler, Stacey: FIC, NIH, Bethesda, MD, USA;
ings from the MAL‐ED study. Matern Child Nutr. 2018;14: Lang, Dennis: FIC, NIH, Bethesda, MD, USA;
e12584. https://doi.org/10.1111/mcn.12584 McCormick, Benjamin: FIC, NIH, Bethesda, MD, USA;
McGrath, Monica: FIC, NIH, Bethesda, MD, USA;
Miller, Mark: FIC, NIH, Bethesda, MD, USA;
Mohale, Archana: FIC, NIH, Bethesda, MD, USA;
APPENDIX A
Nayyar, Gaurvika: FIC, NIH, Bethesda, MD, USA;
M A L ‐ E D I N V E S TI G A T O R S Psaki, Stephanie: FIC, NIH, Bethesda, MD, USA;
Acosta, Angel Mendez: A.B. PRISMA, Iquitos, Peru; Rasmussen, Zeba: FIC, NIH, Bethesda, MD, USA;
Chavez, Cesar Banda: A.B. PRISMA, Iquitos, Peru; Richard, Stephanie: FIC, NIH, Bethesda, MD, USA;
Flores, Julian Torres: A.B. PRISMA, Iquitos, Peru; Seidman, Jessica: FIC, NIH, Bethesda, MD, USA;
Olotegui, Maribel Paredes: A.B. PRISMA, Iquitos, Peru; Wang, Vivian: FIC, NIH, Bethesda, MD, USA;
Pinedo, Silvia Rengifo: A.B. PRISMA, Iquitos, Peru; Blank, Rebecca: FNIH, Bethesda, MD, USA;
Trigoso, Dixner Rengifo: A.B. PRISMA, Iquitos, Peru; Gottlieb, Michael: FNIH, Bethesda, MD, USA;
Vasquez, Angel Orbe: A.B. PRISMA, Iquitos, Peru; Tountas, Karen: FNIH, Bethesda, MD, USA;
Ahmed, Imran: Aga Khan University, Naushahro Feroze, Amour, Caroline: Haydom Lutheran Hospital, Haydom,
Pakistan; Tanzania;
Alam, Didar: Aga Khan University, Naushahro Feroze, Mduma, Estomih: Haydom Lutheran Hospital, Haydom,
Pakistan; Tanzania;
Ali, Asad: Aga Khan University, Naushahro Feroze, Ahmed, Tahmeed: ICDDR‐B, Dhaka, Bangladesh;
Pakistan; Ahmed, A. M. Shamsir: ICDDR‐B, Dhaka, Bangladesh;
Bhutta, Zulfiqar A.: Aga Khan University, Naushahro Feroze, Dinesh, Mondol: ICDDR‐B, Dhaka, Bangladesh;
Pakistan; Tofail, Fahmida: ICDDR‐B, Dhaka, Bangladesh;
Qureshi, Shahida: Aga Khan University, Naushahro Feroze, Haque, Rashidul: ICDDR‐B, Dhaka, Bangladesh;
Pakistan; Hossain, Iqbal: ICDDR‐B, Dhaka, Bangladesh;
Shakoor', Sadia: Aga Khan University, Naushahro Feroze, Islam, Munirul: ICDDR‐B, Dhaka, Bangladesh;
Pakistan; Mahfuz, Mustafa: ICDDR‐B, Dhaka, Bangladesh;
Soofi, Sajid: Aga Khan University, Naushahro Feroze, Chandyo, Ram Krishna: IOM, Tribuhvan University, Kathmandu,
Pakistan; Nepal;
Turab, Ali: Aga Khan University, Naushahro Feroze, Shrestha, Prakash Sunder: IOM, Tribuhvan University, Kathmandu,
Pakistan; Nepal;
Yousafzai, Aisha K.: Aga Khan University, Naushahro Feroze, Shrestha, Rita: IOM, Tribuhvan University, Kathmandu,
Pakistan; Nepal;
Zaidi, Anita K. M.: Aga Khan University, Naushahro Feroze, Ulak, Manjeswori: IOM, Tribuhvan University, Kathmandu,
Pakistan; Nepal;
Bodhidatta, Ladaporn: AFRIMS, Bangkok, Thailand; Black, Robert: JHU, Baltimore, MD, USA;
Mason, Carl J.: AFRIMS, Bangkok, Thailand; Caulfield, Laura: JHU, Baltimore, MD, USA;
Babji, Sudhir: Christian Medical College, Vellore, India; Checkley, William: JHU, Baltimore, MD, USA;
Bose, Anuradha: Christian Medical College, Vellore, India; Chen, Ping: JHU, Baltimore, MD, USA;
John, Sushil: Christian Medical College, Vellore, India; Kosek, Margaret: JHU, Baltimore, MD, USA;
Kang, Gagandeep: Christian Medical College, Vellore, India; Lee, Gwenyth: JHU, Baltimore, MD, USA;
Kurien, Beena: Christian Medical College, Vellore, India; Yori, Pablo Peñataro: JHU, Baltimore, MD, USA;
Muliyil, Jayaprakash: Christian Medical College, Vellore, India; Murray‐Kolb, Laura: Pennsylvania State University, Univer-
Raghava, Mohan Venkata: Christian Medical College, Vellore, India; sity Park, PA, USA;
Ramachandran, Anup: Christian Medical College, Vellore, India; Schaefer, Barbara: Pennsylvania State University, Univer-
Rose, Anuradha: Christian Medical College, Vellore, India; sity Park, PA, USA;
Pan, William: Duke University, Durham, NC, USA; Pendergast, Laura: Temple University, Philadelphia, PA,
Ambikapathi, Ramya: FIC, NIH, Bethesda, MD, USA; USA;
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Abreu, Claudia: Universidade Federal do Ceará, Fortaleza, Svensen, Erling: University of Bergen, Norway; Haydom
Brazil; Lutheran Hospital, Haydom, Tanzania;
Bindá, Alexandre: Universidade Federal do Ceará, Fortaleza, Tor, Strand: University of Bergen, Norway;
Brazil; Patil, Crystal: University of Illinois, Urbana‐Cham-
Costa, Hilda: Universidade Federal do Ceará, Fortaleza, paign, IL, USA;
Brazil; Bessong, Pascal: University of Venda, Thohoyandou,
Di Moura, Alessandra: Universidade Federal do Ceará, Fortaleza, South Africa;
Brazil; Mahopo, Cloupas: University of Venda, Thohoyandou,
Filho, Jose Quirino: Universidade Federal do Ceará, Fortaleza, South Africa;
Brazil; Mapula, Angelina: University of Venda, Thohoyandou,
Leite, Álvaro: Universidade Federal do Ceará, Fortaleza, South Africa;
Brazil; Nesamvuni, Cebisa: University of Venda, Thohoyandou,
Lima, Aldo: Universidade Federal do Ceará, Fortaleza, South Africa;
Brazil; Nyathi, Emanuel: University of Venda, Thohoyandou,
Lima, Noelia: Universidade Federal do Ceará, Fortaleza, South Africa;
Brazil; Samie, Amidou: University of Venda, Thohoyandou,
Lima, Ila: Universidade Federal do Ceará, Fortaleza, South Africa;
Brazil; Barrett, Leah: UVA, Charlottesville, VA, USA;
Maciel, Bruna: Universidade Federal do Ceará, Fortaleza, Gratz, Jean: UVA, Charlottesville, VA, USA;
Brazil; Guerrant, Richard: UVA, Charlottesville, VA, USA;
Moraes, Milena: Universidade Federal do Ceará, Fortaleza, Houpt, Eric: UVA, Charlottesville, VA, USA;
Brazil; Olmsted, Liz: UVA, Charlottesville, VA, USA;
Mota, Francisco: Universidade Federal do Ceará, Fortaleza, Petri, William: UVA, Charlottesville, VA, USA;
Brazil; Platts‐Mills, James: UVA, Charlottesville, VA, USA;
Oria, Reinaldo: Universidade Federal do Ceará, Fortaleza, Scharf, Rebecca: UVA, Charlottesville, VA, USA;
Brazil; Shrestha, Binob: Walter Reed/AFRIMS Research Unit,
Quetz, Josiane: Universidade Federal do Ceará, Fortaleza, Kathmandu, Nepal;
Brazil; Shrestha, Sanjaya Kumar: Walter Reed/AFRIMS Research Unit,
Soares, Alberto: Universidade Federal do Ceará, Fortaleza, Kathmandu, Nepal.
Brazil;