Kismul et al.

BMC Public Health (2018) 18:74

DOI 10.1186/s12889-017-4621-0

RESEARCH ARTICLE Open Access

Determinants of childhood stunting in the

Democratic Republic of Congo: further
analysis of Demographic and Health Survey
2013–14
Hallgeir Kismul1*† , Pawan Acharya2†, Mala Ali Mapatano3 and Anne Hatløy4

Abstract
Background: Prevalence of child stunting in the Democratic Republic of Congo (DRC) is among the highest in the
world. There is a need to systematically investigate how stunting operates at different levels of determination and
identify major factors contributing to the development of stunting. The aim of this study was to look for key
determinants of stunting in the DRC.
Methods: This study used data from the DRC Demographic Health Survey 2013–14 which included anthropometric
measurement for 9030 under 5 year children. Height-for-Age Z score was calculated and classified according to the
WHO guideline. The association between stunting and bio-demographic characteristics was assessed using logistic
regression.
Results: Prevalence of stunting was much higher in boys than girls. There was a significant rural urban gap in the
prevalence of stunting with rural areas having a larger proportion of children living with stunting than urban.
Male children, older than 6 months, preceding birth interval less than 24 months, being from lower wealth quintiles
had the highest odds of stunting. Several provinces had in particular high odds of stunting. Early initiation of
breastfeeding, mother’s age more than 20 years at the time of delivery had lower odds of stunting. The taller the
mother the less likely the child was to be stunted. Similarly, mother’s BMI, access to safe water, access to hygienic
toilet, mother’s education were found negatively correlated with child stunting in the bivariate logistic regression,
but they lost statistical significance in multivariate analysis together with numbers of children in the family and
place of residence.
Conclusions: Child stunting is widespread in the DRC and increasing prevalence is worrisome. This study has
identified modifiable factors determining high prevalence of stunting in the DRC. Policy implementation should in
particular target provinces with high prevalence of stunting and address modifiable determinants such as reducing
socioeconomic disparity. Nutrition promotion intervention, including early initiation of breastfeeding should be an
immediate priority.
Keywords: Child health, Stunting, Chronic malnutrition, Growth disorders, Health status disparities, Social
determinants, The Democratic Republic of Congo, DHS

* Correspondence: [email protected]
†
Equal contributors
1
Centre for International Health, University of Bergen, 5009 Bergen, Norway
Full list of author information is available at the end of the article

© The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0
International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and
reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to
the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver
(http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
Kismul et al. BMC Public Health (2018) 18:74 Page 2 of 14

Background There are to our knowledge only two studies that have
The Democratic Republic of Congo (DRC) has among analysed national data on factors determining children’s
the highest percentages of chronic child malnutrition, or nutritional status in the DRC. A study used data from
stunting, in the world with lasting consequences for the the 2001 DRC Multiple Indicators Cluster Survey (MICS)
children who suffer from this nutritional disorder [1]. to examine the association between maternal education
Stunting during early childhood has several negative and child nutritional status [16]. A second study employed
implications and has been associated with adverse effects data from the 2007 DRC Demographic Health Survey
on cognitive development, school achievement and (DHS) [17]. The study primarily addressed the issue of the
economic productivity in adulthood and maternal re- impact of geographic location on children’s nutritional sta-
productive outcomes [2, 3]. tus. There is therefore no study that uses the more recent
Globally, there has been a significant decline in the data from the DRC-DHS 2013–14 to examine the wide
prevalence of stunting below the age of 5 years. In 1990 range of factors that contribute to the high prevalence of
as much as 40% of children were stunted but in 2015 stunting in the DRC.
the percentage had declined to 24% [1, 4]. While, the The aim of the study is to look for key factors associ-
prevalence of stunting at the global level declined signifi- ated with childhood stunting in the DRC. The study uses
cantly, the decrease has been more modest in sub-Saharan data from the DRC-DHS 2013–14 collected from the na-
Africa. Some sub-Saharan countries have experienced a tionally representative cross-sectional survey conducted
reduction in stunting, other countries have not managed in 2013/14. By identifying key factors determining stunt-
to combat stunting and in these countries chronic malnu- ing the results from our study can be transferred to
trition is widespread with prevalence over 40%. The DRC other settings than the DRC with the findings, especially,
is among these countries and has among the highest being relevant for nutritional initiatives in areas with se-
prevalence of stunting in the region [5]. vere problems of stunting.
Studies across geographical settings show that weight
and length at birth and during the first 5 years of life are
similar across different conditions when mother’s nutri- Methods
tional and health needs are fulfilled and when constraints Survey
on growth are limited [6]. In the same way, under such We analysed data for children below the age of 5 years
conditions the growth of children from different conti- from the DRC-DHS 2013–14 conducted in 2013/14 [18].
nents demonstrates very similar growth patterns [7, 8]. The survey was conducted as a multistage cluster sam-
A number of factors may cause linear growth failure, ple survey. In accordance with the DRC’s administrative
including infections and suboptimal feeding practices. division into provinces the survey divided the country
In addition, various environmental conditions can influence into 26 sampling domains. These domains were further
linear growth during the first years of life, including mater- stratified into urban and rural areas. From the urban
nal nutritional status, access to safe drinking water, hygiene areas neighbourhoods were sampled from cities and towns
and sanitation. There is growing understanding of the rela- whereas for rural areas villages and chiefdoms were sam-
tion between stunting and socio-economic factors. The lit- pled. Subsequently a fixed number of households were
erature has demonstrated social inequalities in nutrition, chosen from each of the selected clusters (Fig. 1). Details
showing that children living in poor households are more of the DHS methodology is elaborated in the measureDHS
likely to be stunted than children from richer households website [19] and the country specific methodology for the
[9–11]. It has been suggested that economic growth in low- DRC DHS 2013–14 is elaborated in the final report (in
income countries is associated with a parallel improvement French) which can be freely downloaded from the measur-
in children’s nutritional status [12, 13]. In order for eco- eDHS website [20].
nomic growth to reduce stunting it needs to improve access The DHS collected anthropometric data for all women
to sanitation, better education for women, increase access and children younger than 5 years in the selected house-
to quality food and reduce social inequalities [14, 15]. hold. In total, 9369 children were measured for their
There are several studies that have examined factors anthropometric indices. Afterwards, based on WHO
associated with child stunting including biological, growth standards, 331 children were excluded because
demographic and social factors. However, there is a need of the extreme HAZ value i.e. HAZ above 6SD or below
for studies that further investigate how stunting operates -6SD and 44 children were excluded for biologically im-
at different levels of determination in order to identify key plausible heights, resulting in 8994 valid measurements.
factors contributing to the development of stunting. In Children who did not sleep last night at their home were
our study, we apply a conceptual framework for determi- futher excluded (n = 110) from the analysis. Therefore, the
nants of malnutrition with the intention of comparing the total number of children included in this analysis was
importance of determinants at different levels. 8884 and after adjusting the cluster design and sample
Kismul et al. BMC Public Health (2018) 18:74 Page 3 of 14

Fig. 1 Multistage sampling procedure, DRC DHS 2013-14

weight the corrected sample size became 9030. WHO Independent variables
child growth standard is a widely used criteria in data The information regarding the background bio-demo-
cleaning while analyzing anthropometric data [21]. A graphic and socioeconomic characteristics of children less
study by using data from 21 DHS countries found WHO than 5 years of age were obtained from interview with their
standard 2006 as the most inclusive criteria resulting mothers. Maternal nutritional status was assessed by BMI,
in the highest reported prevalence compared to other and coded as follow: below 18.5 = malnourished; 18.5–
standards [22]. Since 2006, DHS is using the WHO 2006 24.9 = normal; and BMI ≥25.0 = overweight.
criteria as it started using the WHO 2006 reference popu-
lation to compute the z scores [23].
Analytical framework
We modified the analytical framework from Hien and
Variables Hoa [27]. This framework was based on the UNICEF
Dependent variable conceptual framework describing determinants as tiers
Data regarding the height/length and weight were obtained of interrelations [28–30]. The UNICEF framework clari-
for children below 59 months of age. Height-for-age index fies how the problem of child malnutrition is related to
was calculated according to the WHO-MGRS 2006 Child factors at higher levels and thereby views the problem of
Growth Standards [21]. A z-score of height for age index malnutrition as a larger development problem [31].
(HAZ) < −2SD was defined as stunted. A HAZ between Based on the conceptual framework we grouped the
-2SD and -3SD was considered as moderate stunting, and independent variables into distal, intermediate and prox-
HAZ < −3SD as severe stunting [24–26]. imal factors (Fig. 2).

Fig. 2 Conceptual framework for hierarchial regression modeling of determinants of child nutritional status
Kismul et al. BMC Public Health (2018) 18:74 Page 4 of 14

The distal factors included were mother’s education, in Kasai (Fig. 4). Also, the prevalence of stunting accord-
ethnicity wealth quintile, region/province and urban/rural ing to the provinces is shown in the additional file (See
residence. Intermediate characteristics were: environmen- Additional file 1: Table S1). Detailed distribution of
tal factors such as number of children in the family, family stunting is shown in Table 1.
size, availability of safe water supply and hygienic toilet,
and maternal factors including mother’s age at delivery, Bivariate analysis
preceding birth interval, mother’s BMI and mother’s Bivariate logistic regression analysis showed that age and
height. We included birth order, had diarrhoea within the sex was associated with childhood stunting. Among the
past 14 days and breastfeeding initiated within the first distal factors- mother’s education and wealth quintiles
hour after birth as proximate factors. We kept age and sex were found to be negatively correlated with child stunt-
separately because age and sex might work independently ing. Rural residency and province were also associated
or through the distal, intermediate or proximal factors. with stunting. Intermediate factors including mother’s
age at delivery, mother’s BMI, preceding birth interval,
Statistical analysis number of children in the household were also found
The analysis was performed using STATA 14.0. At first, the to be associated with stunting together with access to
data was set as survey data using “svyset” command by safe water and access to hygienic toilet facility (See
adjusting the cluster design and sample weights. Prevalence Additional file 2: Table S2).
of childhood stunting was calculated using svy: command
prefix [32]. Survey analysis technique is recommended for
DHS data [33]. Differences in stunting prevalence across Hierarchical logistic regression analysis
background characteristics were tested using chi-square test. Distal factors
The association between bio-demographic and socio- Mother’s education was significantly associated in the
economic characteristics with child stunting were assessed first model where the aOR for highly educated mother’s
by three different logistic regression models. Initially, child’s children was 0.45 (95% CI 0.22, 0.93). In the following
age, sex and distal factors were included in the model. In models the statistical significance was lost. In addition
the second model, intermediate factors were added to see stunting was significantly associated with wealth quintile
the effect of distal factors through the intermediate factors. in all the three models. Children from the poorest wealth
Finally, in the third model child specific proximate factors quintile had an aOR = 2.90 (95% CI 1.83, 4.54) for being
were additionally adjusted to the regression analysis. stunted compared to children from the richest wealth
Additionally, a multinomial logistic model was used to quintile. Regarding the provinces, model-3 showed that
estimate the relative risk ratio (RRR) for the severity of children from Kasai, Tshuapa, Kasai-oriental, Sankuru,
stunting according to the background characteristics. Haut-Katanga, and Sud-Kivu provinces had significant
higher odds ratio of stunting in comparison to the chil-
Results dren from Kinshasa province. With regards to residence,
Descriptive analysis urban/rural residence, this variable was not statistically
The prevalence of stunting was 42.7% [95% CI: 41.30, significantly associated with child stunting (Table 2).
44.15] comprising of 20.2% moderate and 22.5% severe
stunting (Table 1). Intermediate factors
Highest prevalence of stunting, 54.0%, was found in Compared to the children with mothers below 20 years
the age group 36–47 months (Fig. 3). Prevalence of of age at childbirth, children with the mothers aged 20–
stunting was significantly higher in boys than in girls 34 years [aOR = 0.70; 95% CI: 0.52, 0.94] and 35 years
with the figures being 45.2% for boys and 40.2% for girls. or more [aOR = 0.65; 95% CI: 0.45, 0.94] had signifi-
The prevalence was higher among the children of cantly lower odds of being stunted.
mothers with little or no education. The prevalence of In comparison to the first born children, the children
stunting among the children whose mother’s didn’t have who had <24 months preceding birth interval had sig-
any school education was 50.8%, on the other hand, the nificantly higher odds ratio of stunting [aOR = 1.38;
prevalence was 13.1% among the children of mothers 95% CI: 1.061.79] (Table 2, model 3).
with higher education. The prevalence among the poor- On the other hand, mother’s Body Mass Index (BMI)
est wealth quintile was 49.7%, which declined to 22.9% and number of children within the family were not signifi-
among the richest wealth quintile. There was a signifi- cantly associated with stunting, however model 2 detected
cant rural urban gap in stunting with 47.2% of children marginally significantly high risk of stunting in children
living in rural areas being stunted versus 32.5% of chil- from large families [aOR = 1.26; 95% CI: 1.00, 1.58].
dren living in urban areas. According to the provinces Environmental factors, including access to safe water
the prevalence ranges from 17.3% in Kinshasa to 57.95% and hygienic toilet had a negative association with
Kismul et al. BMC Public Health (2018) 18:74 Page 5 of 14

Table 1 Sample distribution and prevalence of Stunting among under five year children; the Democratic Republic of Congo 2013–14
Characteristics Sample Moderate Severe Total Stunting(<−2SD)
% n Stunting % Stunting % % 95% CI
Age p < 0.001
< 6 months 10.8 976 8 6.7 14.7 [12.0,17.7]
6–11 months 9.8 888 9.9 13.2 23.1 [18.9,27.8]
12–23 months 18.9 1707 21.4 17.7 39.1 [35.9,42.3]
24–35 months 20.4 1840 23.4 26.8 50.2 [47.1,53.4]
36–47 months 19.7 1783 24.7 29.3 54.0 [50.7,57.3]
48–59 months 20.4 1838 23.2 28.9 52.1 [48.8,55.3]
Total 100 9030 20.2 22.5 42.7 [41.3,44.2]
Sex p < 0.01
Male 50.0 4517 20.4 24.9 45.2 [43.2,47.3]
Female 50.0 4513 20.1 20.1 40.2 [38.2,42.2]
Total 100 9030 20.2 22.5 42.7 [41.3,44.2]
Distal factors
Mother's education p < 0.001
None 19.7 1641 20.1 30.6 50.8 [47.5,54.0]
Primary 43.7 3632 21.3 25.8 47.1 [44.8,49.4]
Secondary 35.4 2945 20.1 13.1 33.2 [30.9,35.6]
Higher 1.2 97 9.8 3.3 13.1 [7.3,22.5]
Total 100 8315 20.5 22.0 42.5 [41.0,44.0]
Wealth quintile p < 0.001
Richest 16.1 1456 14.0 9.0 22.9 [20.2,26.0]
Richer 18.5 1671 20.4 21.0 41.4 [37.9,45.0]
Middle 20.4 1843 22.3 23.5 45.8 [42.6,49.0]
Poorer 22.4 2018 22.2 26.1 48.3 [45.1,51.5]
Poorest 22.6 2042 20.8 28.8 49.7 [46.9,52.5]
Total 100 9030 20.2 22.5 42.7 [41.3,44.2]
Residence p < 0.001
Urban 30.2 2728 18.7 13.8 32.5 [30.3,34.7]
Rural 69.8 6302 20.9 26.2 47.2 [45.4,49.0]
Total 100 9030 20.2 22.5 42.7 [41.3,44.2]
Intermediate factors
Mothers age at delivery p = 0.084
< 20 years 14.5 1307 24.0 22.5 46.5 [43.0,50.1]
20–34 years 63.2 5704 19.9 22.0 41.9 [40.1,43.7]
> =35 years 22.4 2020 18.9 23.8 42.6 [39.6,45.7]
Total 100 9030 20.2 22.5 42.7 [41.3,44.2]
Mother’s body mass index p < 0.001
Thin 11.8 944 22.7 22.8 45.4 [41.0,50.0]
Normal 72.6 5829 20.8 23.3 44.1 [42.4,45.9]
Overweight 15.6 1252 17.4 15.7 33.1 [29.5,36.8]
Total 100 8025 20.5 22.0 42.6 [41.1,44.1]
Birth interval p < 0.001
First Birth 18.1 1470 21.9 19.1 41.0 [37.7,44.4]
Kismul et al. BMC Public Health (2018) 18:74 Page 6 of 14

Table 1 Sample distribution and prevalence of Stunting among under five year children; the Democratic Republic of Congo 2013–14
(Continued)
< 24 months 21.6 1755 18.9 29.4 48.3 [44.9,51.8]
24–47 months 47.35 3856 21.3 21.1 42.4 [40.3,44.6]
48 months or more 13.1 1063 17.8 17.0 34.7 [30.9,38.8]
Total 100 8143 20.4 22.0 42.4 [40.9,43.9]
Family size p = 0.532
Small(<4) 22.3 1711 21.6 20.3 41.8 [38.7,45.1]
Medium (4–6 members) 17.0 1303 19.3 21.7 41.0 [37.4,44.6]
Large (>8 members) 60.7 4660 19.2 24.0 43.2 [41.2,45.2]
Total 100 7674 19.7 22.8 42.5 [41.0,44.06]
Number of Children p < 0.5
1 20.0 1806 22.0 17.5 39.5 [36.5,42.7]
2 44.6 4028 20.7 23.2 43.9 [41.7,46.1]
3 26.5 2394 19.2 25.5 44.7 [41.9,47.5]
4 or more 0.9 79 17.7 21.6 39.3 [34.6,44.2]
Total 100 9030 20.2 22.5 42.7 [41.3,44.2]
Access to safe water 0 p < 0.001
No 70.6 6372 21.5 25.0 46.5 [44.8,48.1]
Yes 29.4 2658 17.3 16.4 33.8 [31.4,36.6]
Total 100 9030 20.2 22.5 42.7 [41.3,44.2]
Access to hygienic toilet 0 p < 0.001
No 96.5 8717 20.6 23.1 43.7 [42.2,45.2]
Hygienic 3.5 313 10.1 5.5 15.6 [11.0,21.6]
Total 100 9030 20.2 22.5 42.7 [41.3,44.2]
Proximal factors
Birth order p = 0.113
1 18.0 1476 21.9 19.1 41.0 [37.7,44.4]
2 16.5 1352 20.5 19.2 39.7 [36.3,43.3]
> =3 65.5 5363 20.0 23.5 43.6 [41.7,45.5]
Total 100 8192 20.5 22.1 42.5 [41.0,44.0]
Had Diarrhoea p = 0.441
No 82.4 6691 20.6 22.2 42.8 [41.2,44.5]
Yes 17.6 1430 19.8 21.4 41.2 [37.7,44.9]
Total 100 8121 20.5 22.0 42.5 [41.0,44.0]
Breastfeeding within first hour p = 0.120
No 55.6 4459 22.1 21.5 43.6 [41.6,45.7]
Yes 44.4 3566 18.3 22.9 41.2 [39.0,43.4]
Total 100 8025 20.4 22.1 42.5 [41.0,44.1]
p p-value using chi-square test, CI confidence interval

stunting in unadjusted analysis but lost significance in higher in every age category in comparison to
the multivariate analysis. <6 months children. Regarding the sex difference, the
aOR among female child was significantly lower
Proximal factors [aOR = 0.81; 95% CI: 0.70, 0.94] compared to their
Results of the hierarchical modelling found age and male counterparts.
sex consistently associated with stunting. In the final Breastfeeding initiated within the first hour after birth
model, the adjusted odds ratio were significantly was found protective against child stunting [aOR = 0.82;
Kismul et al. BMC Public Health (2018) 18:74 Page 7 of 14

Fig. 3 Prevalence of child stunting according to age (DRC 2013/14)

95% CI: 0.70, 0.95] in the final model while birth order Indicator Cluster Survey 2001 (MICS-2001), the preva-
and history of diarrhoea showed no significant effect. lence has increased from 33% [34] to 43% in 2014. We
Also, the relative risk ratios (RRR) of moderate and se- found a noteworthy increment in the prevalence of
vere stunting according to background characteristics stunting among the children from the poorest household
are included as supplementary material. (See Additional from 43% in 2001 to [34] 50% in 2013/14. A large pro-
file 3: Table S3). portion of children in the DRC are also suffering from
wasting (low weight-for-height) and underweight (low
Discussion weight-for-age) with the figures from the DRC DHS
In our study, we have used nationally representative data 2013–14 being 7.9 and 22.6% respectively [5].
on the population of the DRC. More than 2 in every five In our study we apply a conceptual framework for de-
children being stunted is a serious public health problem scribing determinants of stunting and in our analysis we
in the DRC. Compared to the result of Multiple distinguish between three levels of determinants namely,

Fig. 4 Prevalence of child stunting across the regions (DRC 2013/14)

Kismul et al. BMC Public Health (2018) 18:74 Page 8 of 14

Table 2 Hierarchical logistic regression analysis of associations between stunting and sociodemographic and clinical factors in
under-five children, the Democratic Republic of Congo, 2013–14
Characteristics Model 1 Model 2 Model 3
aOR 95% CI aOR 95% CI aOR 95% CI
Age
< 6 months 1.00 1.00 1.00
6–11 months 1.89 1.12 3.19 * 1.84 1.07 3.19 * 1.84 1.09 3.13 *
12–23 months 4.22 3.07 5.80 *** 4.35 3.14 6.03 *** 4.41 3.19 6.09 ***
24–35 months 6.59 4.84 8.97 *** 6.34 4.60 8.74 *** 6.53 4.73 9.00 ***
36–47 months 7.93 5.77 10.89 *** 8.78 6.41 12.03 *** 9.60 6.97 13.21 ***
48–59 months 7.67 5.61 10.50 *** 7.63 5.59 10.42 *** 8.13 5.93 11.15 ***
Sex
Male 1.00 1.00 1.00
Female 0.80 0.70 0.92 ** 0.81 0.70 0.94 ** 0.81 0.70 0.94 **
Distal factors
Mother's education
None 1.00 1.00 1.00
Primary 1.03 0.88 1.21 1.02 0.86 1.21 0.99 0.83 1.18
Secondary 0.80 0.67 0.96 * 0.84 0.68 1.03 0.83 0.67 1.04
Higher 0.45 0.22 0.93 * 0.64 0.31 1.32 0.63 0.31 1.28
Wealth quintile
Richest 1.00 1.00 1.00
Richer 2.14 1.57 2.92 *** 1.92 1.32 2.79 ** 1.91 1.32 2.76 **
Middle 2.84 1.98 4.07 *** 2.30 1.51 3.50 *** 2.38 1.56 3.62 ***
Poorer 3.28 2.23 4.83 *** 2.43 1.54 3.82 *** 2.48 1.57 3.92 ***
Poorest 3.93 2.70 5.72 *** 2.81 1.78 4.44 *** 2.90 1.83 4.57 ***
Ethnicity
Bakongo 1.00 1.00 1.00
Bas-kasai et kwilu-kwngo 0.93 0.52 1.67 0.82 0.45 1.49 0.92 0.51 1.66
Cuvette central 0.77 0.41 1.45 0.60 0.31 1.14 0.65 0.34 1.24
Ubangi et itimbiri 1.02 0.53 1.96 1.07 0.53 2.17 1.11 0.54 2.24
Uele lac albert 1.08 0.52 2.24 0.99 0.45 2.18 1.05 0.48 2.30
Basele-k, man. et kivu 0.96 0.45 2.05 0.91 0.41 2.01 0.93 0.41 2.11
Kasai, katanga, Tanganyika 1.00 0.54 1.85 0.94 0.49 1.79 1.08 0.57 2.05
others (lunda/pygmy/foreign) 1.28 0.62 2.68 1.23 0.60 2.50 1.61 0.83 3.13
Residence
Urban 1.00 1.00
Rural 0.92 0.74 1.15 0.90 0.69 1.18 0.89 0.68 1.16
Province (New)
Kinshasa 1.00 1.00
Kwango 1.81 0.93 3.50 1.62 0.78 3.36 1.42 0.69 2.91
Kwilu 1.29 0.73 2.27 1.41 0.74 2.67 1.29 0.69 2.43
Mai-ndombe 1.07 0.59 1.92 1.12 0.61 2.03 1.02 0.56 1.84
Kongo central 2.09 0.97 4.48 1.64 0.72 3.72 1.77 0.84 3.77
Equateur 0.58 0.27 1.24 0.60 0.26 1.40 0.55 0.24 1.28
Mongala 0.96 0.52 1.79 0.84 0.41 1.73 0.79 0.39 1.61
Kismul et al. BMC Public Health (2018) 18:74 Page 9 of 14

Table 2 Hierarchical logistic regression analysis of associations between stunting and sociodemographic and clinical factors in
under-five children, the Democratic Republic of Congo, 2013–14 (Continued)
Nord-ubangi 1.22 0.60 2.51 1.33 0.61 2.91 1.23 0.56 2.69
Sud-ubangi 1.22 0.62 2.42 1.00 0.48 2.08 0.95 0.46 1.96
Tshuapa 1.71 0.86 3.41 2.54 1.24 5.18 * 2.33 1.15 4.72 *
Kasai 2.82 1.60 4.97 *** 3.05 1.65 5.61 *** 2.75 1.49 5.07 **
Kasai-central 1.89 1.02 3.49 * 1.74 0.88 3.46 1.48 0.74 2.96
Kasai-oriental 1.80 1.03 3.15 * 2.05 1.14 3.70 * 1.86 1.04 3.33 *
Lomami 1.97 1.11 3.50 * 1.92 1.00 3.68 P = 0.05 1.64 0.86 3.11
Sankuru 2.49 1.32 4.69 ** 3.11 1.54 6.30 ** 2.87 1.41 5.82 **
Haut-katanga 2.84 1.72 4.69 *** 2.55 1.46 4.46 ** 2.19 1.26 3.81 **
Haut-lomami 1.77 0.95 3.30 1.28 0.63 2.57 1.13 0.57 2.25
Lualaba 1.60 0.85 2.99 1.33 0.62 2.85 1.09 0.47 2.49
Langanyka 1.92 1.04 3.57 * 1.57 0.78 3.17 1.32 0.67 2.62
Maniema 1.70 0.79 3.63 1.42 0.61 3.34 1.37 0.55 3.43
Nord-kivu 2.49 1.29 4.79 ** 2.04 0.97 4.29 2.09 0.98 4.47
Bas-uele 1.30 0.68 2.50 1.48 0.65 3.37 1.07 0.47 2.47
Haut-uele 1.41 0.60 3.32 1.56 0.62 3.91 1.40 0.55 3.52
Ituri 1.53 0.77 3.07 1.33 0.61 2.89 1.37 0.64 2.93
Tshopo 1.19 0.56 2.50 1.25 0.54 2.92 1.17 0.51 2.68
Sud-kivu 3.10 1.45 6.61 ** 2.57 1.15 5.73 * 2.54 1.11 5.83 *
Intermediate factors
Mothers age at delivery
< 20 years 1.00 1.00
20–34 years 0.78 0.59 1.03 0.70 0.52 0.94 *
> =35 years 0.76 0.54 1.06 0.65 0.45 0.94 *
Mother’s body mass index
Thin 1.00 1.00
Normal 0.96 0.73 1.26 0.97 0.74 1.28
Overweight 0.73 0.49 1.10 * 0.73 0.48 1.09
Mother’s height 0.99 0.99 1.00 *** 0.60 0.53 0.68 ***
Birth interval
First Birth 1.00 1.00
< 24 months 1.17 0.86 1.59 1.38 1.06 1.79 *
> 24 months 1.05 0.79 1.40 1.23 0.95 1.59
Family size
Small(<4) 1.00 1.00
Medium (4–6 members) 0.91 0.69 1.19 0.92 0.70 1.21
Large (>8 members) 1.26 1.00 1.58 P = 0.05 1.18 0.93 1.48
Number of Children
1 1.00 1.00
2 1.08 0.87 1.35 1.09 0.88 1.36
3 1.21 0.93 1.59 1.21 0.92 1.58
4 or more 0.98 0.69 1.39 0.99 0.70 1.41
Access to safe water 0.92 0.69 1.23 0.89 0.67 1.19
Access to hygienic toilet 0.80 0.49 1.31 0.80 0.48 1.31
Kismul et al. BMC Public Health (2018) 18:74 Page 10 of 14

Table 2 Hierarchical logistic regression analysis of associations between stunting and sociodemographic and clinical factors in
under-five children, the Democratic Republic of Congo, 2013–14 (Continued)
Proximal factors
Birth order
1 1.00
2 0.74 0.49 1.13
> =3 1.01 0.64 1.57
Had diarrhea
No 1.00
Yes 1.11 0.89 1.39
Breastfeeding within first hour
No 1.00
Yes 0.82 0.70 0.95 **
Model 1: Adjusted for child’s age, sex, and distal factors (mother’s education, ethnicity, place of residence and ecological zone)
Model 2: In addition to model 2, adjusted intermediate factors (mother’s age at delivery, birth interval, mother’s BMI, Mother’s height, size of family, number of
children in family, access to safe water, and access to hygienic toilet)
Model 3: In addition to model 3, adjusted for proximal factors (birth order, diarrhea within past 2 weeks and initiation of breastfeeding within first hour after birth)
OR odds ratio, aOR adjusted odds ratio, CI confidence interval
*
p < 0.05; **p < 0.01; ***p < 0.001

distal, intermediate and proxy factors. In this discussion land in South Kivu is fertile, but shortage of land and land-
we assess and compare the strengths of association be- lessness are problems closely related to food insecurity
tween stunting and different determinants. In this man- and chronic malnutrition. Several provinces with high
ner we identify key determinants and single out at what odds of stunting face problems due to influx of internal as
levels of determination they operate. Our findings are well as refugees from neighbouring countries. The DRC is
contrasted with the results from several other studies characterised by widespread food insecurity and with se-
that have investigated determinants of stunting. This is vere food insecurity in the above provinces.
done in order to establish an understanding of how our Findings from other studies have also highlighted
findings match with existing knowledge in this field. within-country variability in terms of prevalence of mal-
nutrition and the importance of identifying areas with
Distal factors particular high prevalence of malnutrition [35, 36]. The
A major finding is that stunting is above all associated importance of analysing geographically inequalities in
with factors at the distal level. First, we found a strong malnutrition is also supported by a study from the DRC
relationship between stunting and province and second, using the 2013–14 DRC-DHS and data from the 11 old
stunting was found to be strongly associated with socio- provinces. The study demonstrated how malnutrition in
economic status. the DRC related to geographic location. A major finding
In 2016 the DRC was divided into 26 provinces and was that stunting rates was highest in the provinces that
we investigated stunting in these new provinces. Exam- rely on artisanal mining compared to the level observed
ining stunting in these provinces reveals that there are a in the eastern provinces affected by civil war. Our focus
number of distal factors that can be related to higher on the new provinces allows a focus on relatively smaller
odds of stunting. Sankuru province had the highest odds geographical units and thereby we are in a relatively
of stunting. This is a landlocked province and with poor good position to elicit the variety of factors that contrib-
road system and no railway, the area is extremely diffi- ute to regional inequalities in stunting.
cult to reach. Manufactured goods including food items In addition to finding a strong relationship between
are sold at increasingly higher prices while cash crop- stunting and province our research further confirms the
ping is hard to develop. Kasai is another province with a strong relationship between stunting and socio-economic
higher odds of stunting. The major livelihood in the inequality. This study showed that the children living in
province is artisanal mining, especially diamond mining. the poorest household had higher odds of being stunted.
During the last 15 years, the diamond sector has been In contrast the highest proportion of children with
influenced by declining international markets. In addition, stunting in the DRC were categorised in the middle
people tend to neglect food production and the province group in 2007 and 2010 [37, 38]. The literature has
has to import much of its food. Provinces affected by war, demonstrated important socio-economic inequalities in
including South Kivu, have also high odds of stunting. The child malnutrition showing that children living in
Kismul et al. BMC Public Health (2018) 18:74 Page 11 of 14

poorer households are likely to be more stunted than clean water and hygienic toilet we did not find any statisti-
children in better-off households [9–11, 39]. Higher so- cally significant relationships between stunting and these
cioeconomic position is likely to represent better living factors.
conditions which again contributes to better child care Our study revealed that about one fourth of mothers
and feeding practices and improved access to food and were teenagers at the time of their recent delivery and
a potential decline in the occurrence of different forms the multivariate analysis showed that children who had
of malnutrition [40]. mothers whose age was above 20 years at delivery were
Whereas we found strong relationships between stunt- less likely to suffer from stunting than children with
ing and regional and social inequalities the relationships teenager mothers. Similar results were reported by a
between stunting and others factors at the distal level prospective study from five low-income countries [51].
are unclear. This concerns the relationship between Early marriage might have contributed most for a such
stunting and place of residence as well as the relation- high proportion of teenage mothers [52, 53]. Early child
ship between stunting and mother’s education. birth represents a health risk both for mothers and chil-
We found that the largest proportion of children with dren and has negative consequences for the growth of
stunting lived in rural households. On the other hand, in the child [54]. During maternal growth there might be a
the multivariate analysis we did not find any statistically competition of scarce nutrients between the mother and
significant association between place of residence and the foetus and this competition might result in early
stunting. Our findings thereby contradict findings from childhood undernutrition and also increase negative im-
other studies. These studies have found that place of plications of maternal malnutrition [55].
residence can explain variations in prevalence of child Our research demonstrates a relationship between
malnutrition [17, 41] and that there are evidences that in stunting and birth intervals and we found, in model 3,
low-income countries, rural children are at a higher risk of that a birth interval below 24 months was associated
malnutrition than their urban counterparts [42–44]. Then with statistically significant higher odds of stunting than
again our results are in accordance with research reporting longer birth intervals. The relationship between birth
that when controlling for potential confounders the odds intervals and children’s nutritional status has been investi-
of being stunting were not significantly different between gated and some studies have in accordance with our find-
children living in rural or urban areas [45]. ings found short intervals to adversely affect the child’s
We also assessed how stunting was related to mothers’ nutritional status [56–58]. Still a review examining this re-
education. The crude logistic regression showed a highly lationship concluded that the reduction in stunting found
significant negative correlation between mother’s educa- in some studies could be due to residual confounding fac-
tion and child stunting, however, the multivariate ana- tors not covered in the analysis including breastfeeding
lysis, model 2 and 3, showed that children of mothers and maternal height [59]. In our analysis we controlled for
who had secondary and higher education were less likely these factors and found short birth intervals to be associ-
to be stunted than children who had mothers with no ated with stunting.
education and mothers with only primary education, but Our findings demonstrate a higher risk of stunting
without statistical significance. Our findings apparently among the children of mothers with short heights. Our
contrast the results of other similar studies that have findings thereby corroborate with previous studies show-
demonstrated significant relationship between mother’s ing similar results [60–62]. One explanation of maternal
education and child nutrition [46–50]. On the other height to child stunting relationship is that mothers with
hand the results from a study from the DRC using short stature have a higher risk of giving birth of babies
DRC MICS 2001 data are uncertain [16]. It found that with low birth weight [63] which in return are at higher
stunting was higher among the children whose mother risk of poor growth during childhood [64].
had secondary education or higher. This association In our study, we found children living in households
disappeared or appeared only after controlling for the with access to safe drinking water were less likely to be
province of residence. stunted and so were children living in households with
access to hygienic toilet, but this association disappeared
Intermediate factors when we controlled for potential confounding factors. In
Our analysis demonstrated strong relationships between our model 3, the strength of association was reduced
stunting and selected factors at the distal level, including and lost statistical significance. Our findings are thereby
regional and social inequalities. On the other hand we not fully in accordance with other studies in this field.
found the associations between stunting and variables at These studies have found evidence that improvement in
the intermediate level to be weaker including the associ- access to clean water, sanitation and hygienic facilities
ation between stunting and mother’s age at delivery, birth have a positive influence on the linear growth of chil-
intervals and mother’s height. With regards to access to dren [65–67].
Kismul et al. BMC Public Health (2018) 18:74 Page 12 of 14

Proximal factors of early initiation of breastfeeding. There are some issues

At the proximal level we examined several variables and raised in our study not directly dealt with in the policy
their relationships with stunting including birth order, document, these include the problem of early age at deliv-
diarrhoea and early initiation of breastfeeding. Stunting ery and short birth intervals. Furthermore we will point
was related to early initiation of breastfeeding but not out the importance of policy implementation attending to
the other variables. The association between stunting the issue of within-country variability in stunting.
and early initiation of breastfeeding was in comparison The government agency PRONAUT (Programme Natio-
with factors at the distal level weak. nale de Nutrition) is taking a lead in implementing the
Other studies have also reported early initiation of nutritional policy. It is present in all provinces. The or-
breastfeeding to protect against stunting early in child- ganisation is especially making efforts to step up its ac-
hood [68]. There are a number of benefits of early breast- tivities in provinces that due to financial constraints
feeding. Colostrum is rich in protective factors and early receive insufficient support including seven of the new
initiation of breastfeeding ensures that the infant receives provinces.
colostrum. Studies have shown that pre-lacteal feeding in-
creases the risk of partial breastfeeding during the first
6 months which again has been associated with stunting Conclusions
[69, 70]. Chronic malnutrition is widespread in the DRC and
At the proximal level, we also dealt with the issue of comparing with previous studies there was an increase
age of growth faltering and prevalence of stunting at in the proportion of children suffering from stunting.
different ages. Whereas the literature has focused on We have identified key factors that can explain contin-
stunting at very early ages, our study shows that the ued and high prevalence of child stunting. Several vari-
prevalence of stunting increases further after the age of ables were associated with stunting and the results of
2 years. This is in accordance with the findings of another our research demonstrate, in a setting with widespread
study from the DRC analysing data from the DRC -DHS child stunting, the importance of addressing determi-
2007 [17]. This finding highlights the important relation- nants at the distal level. First, stunting was strongly asso-
ship between stunting and inappropriate diet also at the ciated with regional inequalities. These regional
age above 2 years. Growth faltering at these ages could be inequalities could be related to a number of distal factors
a consequence of children above the age of 2 years being including the province being landlocked, economic
fed with food characterised by monotony and little variety. adaptation, influx of refugees and war. Second, poverty
was closely connected to high prevalence of stunting
Nutritional policy considerations with the risk of stunting being very high for children liv-
Our findings raise a number of issues for nutritional policy ing in the poorest households. This study, therefore
consideration. The DRC nutritional policy is described in demonstrates the importance of giving priority to identi-
a government document from 2014 and it is this docu- fying pockets of stunting and geographical targeting of
ment that currently guides policy implementation [71]. nutrition programmes. Geographical targeting should be
The document recognises that undernutrition has many combined with a strategy that addresses social inequal-
causes and that efforts to address it must be multisectoral ities in stunting and our study reconfirms the import-
with the government further developing partnerships with ance of nutritional interventions especially targeting
other agencies. It acknowledges the importance of decen- vulnerable groups. In addition to identifying key factors,
tralisation and ensuring that all parts of the country share this study found several intermediate and proximal fac-
equal access nutritional services. Particular attention is tors associated with stunting. These factors cover vari-
paid to vulnerable groups living in disadvantaged environ- ous modifiable determinants such as: early initiation of
ments. In terms of child undernutrition, specific strategies breastfeeding, short birth intervals and mother’s young
have been developed for different age groups outlining age at delivery. These determinants should be incorpo-
a number of interventions required to prevent under- rated in nutritional intervention programs.
nutrition among these groups. Examples of key areas
are; promoting early initiation of breastfeeding, exclusive
breastfeeding during the first 6 months, introduction of
Additional files
complementary feeding at 6 months, continued breast-
feeding up to the age of 2 years as well as addressing Additional file 1: Table S1. Sample distribution and prevalence of
micronutrient deficiencies. The results of our study sup- stunting among under 5 year children according to provinces; DRC.
port the national policy and worth mentioning is the pol- (XLSX 13 kb)
icy’s emphasis on decentralisation, giving special attention Additional file 2: Table S2. Unadjusted odds of stunting among under
five children in DR Congo 2013–14. (XLSX 14 kb)
to vulnerable groups as well as underlining the importance
Kismul et al. BMC Public Health (2018) 18:74 Page 13 of 14

Additional file 3: Table S3. Relative Risk Ratios for moderate and Received: 2 December 2016 Accepted: 21 July 2017
severe Stunting among under 5 year children in DR Congo 2013–14.
(XLSX 17 kb)

References
Abbreviations 1. UNICEF. The state of the world’s children 2016: a fair chance for every child.
aOR: adjusted odds ratio; BMI: body mass index; CI: confidence interval; New York: United Nations Children's Fund (UNICEF); 2016.
DHS: Demographic Health Survey; DRC: Democratic Republic of Congo; 2. Victora CG, Adair L, Fall C, Hallal PC, Martorell R, Richter L, Sachdev HS.
HAZ: height for age z-score; MGRS: Multicentre Growth Reference Study; Study MCU: Maternal and child undernutrition 2 - maternal and child
MICS: Multiple indicator cluster survey; OR: odds ratio; RRR: relative risk ratio; undernutrition: consequences for adult health and human capital. Lancet.
SD: standard deviation; UNICEF: United Nations Children’s Fund; WHO: World 2008;371(9609):340–57.
Health Organization 3. Black RE, Victora CG, Walker SP, Grp MCNS: Maternal and child nutrition study
group. Maternal and child undernutrition and overweight in low-income and
Acknowledgements middle-income countries (vol 382, pg 427, 2013). Lancet. 2013;382(9890):396.
The authors would like to thank measure DHS program for providing access 4. de Onis M, Blossner M, Borghi E. Prevalence and trends of stunting among
to the dataset for this study. The authors would also like to appreciate pre-school children, 1990-2020. Public Health Nutr. 2012;15(1):142–8.
mothers of under-5 year children for providing related information during 5. République Démocratique du Congo. Enquête Démographique et de Santé
the survey. The authors acknowledge the Center for International Health of (EDS-RDC) République Démocratique du Congo 2013–14. Kinshasa:
Bergen in Norway for all the support we have received to this research. We Ministère du Plan avec la collaboration du Ministère de la Santé; 2014.
would like to thank C. Swinger and S.G. Hinderaker for their comments on 6. Villar J, Papageorghiou AT, Pang R, Ohuma EO, Ismail LC, Barros FC, Lambert
the earlier versions of this manuscript. A, Carvalho M, Jaffer YA, Bertino E, et al. The likeness of fetal growth and
newborn size across non-isolated populations in the INTERGROWTH-21st
Funding project: the fetal growth longitudinal study and newborn cross-sectional
No specific funding was received for this study. study. Lancet Diabetes Endocrinol. 2014;2(10):781–92.
7. Victora CG, de Onis M, Garza C, Cole T, Frongillo EA, Cameron N, Shekar M,
Availability of data and materials Yip R, Bhatnagar S, Burger H, et al. Growth patterns of breastfed infants in
Dataset for this analysis can be accessed with the request to MeasureDHS seven countries. Acta Paediatr. 2000;89(2):215–22.
program. http://dhsprogram.com/data/dataset/Congo-Democratic- 8. Bhandari N, Bahl R, Taneja S, de Onis M, Bhan MK. Growth performance of
Republic_Standard-DHS_2013.cfm?flag=0 After the permission, datasets can affluent Indian children is similar to that in developed countries. B World
be freely downloaded from the DHS data archive. Health Organ. 2002;80(3):189–95.
9. Zere E, McIntyre D. Inequities in under-five child malnutrition in South
Authors’ contributions Africa. Int J Equity Health. 2003;2(1):7.
HK and PA conceptualized the study, performed statistical analysis, 10. Van de Poel E, Hosseinpoor AR, Jehu-Appiah C, Vega J, Speybroeck N.
interpreted the results and prepared first draft of the manuscript. MAM and Malnutrition and the disproportional burden on the poor: the case of
HA contributed in the revision of manuscript. All authors agreed on the final
Ghana. Int J Equity Health. 2007;6:21.
version of the manuscript.
11. Hong R. Effect of economic inequality on chronic childhood undernutrition
in Ghana. Public Health Nutr. 2007;10(4):371–8.
Ethics approval and consent to participate
12. Pritchett L, Summers LH. Wealthier is healthier. J Hum Resour. 1996;31(4):841–68.
This study was based on the secondary data from Demographic and Heath
13. Smith LC, Haddad L. How potent is economic growth in reducing
Survey, DRC (2013–14). The survey was approved by Ethics Committee of the
undernutrition? What are the pathways of impact? New cross-country
School of Public Health (ESP) of the University of Kinshasa and the ICF
evidence. Econ Dev Cult Chang. 2002;51(1):55–76.
International Institutional Review Board. Informed consent was obtained
14. Nisbett N, Gillespie S, Haddad L, Harris J. Why worry about the politics of
from the respondent to participate in the survey before the interview was
childhood Undernutrition? World Dev. 2014;64:420–33.
conducted. A special statement was included in the beginning of the
15. Smith LC, Haddad L. Reducing child Undernutrition: past drivers and
household and the individual questionnaire. This statement explained the
priorities for the post-MDG era. World Dev. 2015;68:180–204.
purpose of the study. Participation in the survey was completely voluntary
16. Emina JO, Kandala N-B, Inungu J, Yazoume Y. Maternal education and child
and the respondents were informed that they had the right to refuse to
nutritional status in the Democratic Republic of Congo. J Public Health
answer any questions or stop the interview at any point. The informed
Epidemiol. 2011;3(12):576–92.
consent statement was read exactly as it was written before the respondents
17. Kandala NB, Madungu TP, Emina JBO, Nzita KPD, Cappuccio FP. Malnutrition
were asked to participate in the interview. Then the interviewer signed their
among children under the age of five in the Democratic Republic of Congo
names attesting to the fact that he/she read the consent statement to the
(DRC): does geographic location matter? BMC Public Health. 2011;11:261.
respondent. No written consent was obtained because the information
18. République Démocratique du Congo. Enquête Démographique et de Santé
requested was neither controversial nor sensitive. Measure DHS program
(EDS-RDC) 2013–2014. Kinshasa: Ministère du Plan et Suivi de la Mise en
permitted access to the secondary data for this study.
oeuvre de la Révolution de la Modernité; 2014.
19. DHS Methodoogy [http://dhsprogram.com/What-We-Do/Survey-Types/DHS-
Consent for publication
Methodology.cfm]. Accessed 19 June 2017.
Not applicable.
20. Congo Democratic Republic: Standard DHS, 2013–14 [http://dhsprogram.
com/what-we-do/survey/survey-display-421.cfm]. Accessed 19 June 2017.
Competing interests
The authors declare that they have no competing interests. 21. Child Growth Standards: Length/Height-for-Age, Weight-for-Age, Weight
for- Length, Weight-for-Height and Body Mass Indexfor-Age: Methods and
Development [http://www.who.int/childgrowth/standards/Technical_report.
Publisher’s Note pdf]. Accessed 24 Oct 2017.
Springer Nature remains neutral with regard to jurisdictional claims in 22. Crowe S, Seal A, Grijalva-Eternod C, Kerac M. Effect of nutrition survey
published maps and institutional affiliations. ‘cleaning criteria’ on estimates of malnutrition prevalence and disease
burden: secondary data analysis. PeerJ. 2014;2:e380.
Author details 23. Shireen A, Kothari MT, Pullum T. An assessment of the quality of DHS
1
Centre for International Health, University of Bergen, 5009 Bergen, Norway. anthropometric data, 2005-2014. In: DHS methodological reports no 16.
2
Nepal Development Society, Bharatpur, Chitwan, Nepal. 3Department of Rockville: ICF International; 2015.
Nutrition, School of Public Health, University of Kinshasa, Kinshasa 1, 24. WHO: Nutrition Landscape Information System (NLIS) country profile indicators:
Democratic Republic of Congo. 4Fafo, Institute for Labour and Social interpretation guide. 2010. Geneva: World Health Organization; 2010.
Research, Box 2947 Toyen, 0608 Oslo, Norway. 25. Rutstein SO, Rojas G. Guide to DHS statistics. Calverton: ORC Macro; 2006.
Kismul et al. BMC Public Health (2018) 18:74 Page 14 of 14

26. Bullen PAB. The positive deviance/hearth approach to reducing child age at childbirth and child and adult outcomes in the off spring: a
malnutrition: systematic review. Tropical Med Int Health. 2011;16(11):1354–66. prospective study in five low-income and middle-income countries
27. Hien NN, Hoa NN. Nutritional status and determinants of malnutrition in (COHORTS collaboration). Lancet Glob Health. 2015;3(7):E366–77.
children under three years of age in Nghean, Vietnam. Pak J Nutr. 2009; 52. Child marriage rates the Democratic Republic of Congo [http://www.
8(7):958–64. girlsnotbrides.org/child-marriage/democratic-republic-of-the-congo/].
28. Bellamy C. The state of the World's children 1998: focus on nutrition. Accessed 24 Oct 2016.
Geneva: The United Nations Children's Fund (UNICEF); 1998. 53. Raj A, Saggurti N, Winter M, Labonte A, Decker MR, Balaiah D, Silverman JG.
29. Engle PL, Menon P, Haddad L. Care and nutrition: concepts and The effect of maternal child marriage on morbidity and mortality of
measurement. World Dev. 1999;27(8):1309–37. children under 5 in India: cross sectional study of a nationally representative
30. Levitt EJ, Pelletier DL, Pell AN. Revisiting the UNICEF malnutrition framework sample. Brit Med J. 2010;340:b4258.
to foster agriculture and health sector collaboration to reduce malnutrition: 54. Ganchimeg T, Ota E, Morisaki N, Laopaiboon M, Lumbiganon P, Zhang J,
a comparison of stakeholder priorities for action in Afghanistan. Food Policy. Yamdamsuren B, Temmerman M, Say L, Tuncalp O, et al. Pregnancy and
2009;34(2):156–65. childbirth outcomes among adolescent mothers: a World Health
31. Black RE, Allen LH, Bhutta ZA, Caulfield LE, de Onis M, Ezzati M, Mathers C, Organization multicountry study. Bjog-Int J Obstet Gy. 2014;121:40–8.
Rivera J, Study MCU. Maternal and child undernutrition 1 - maternal and 55. Lenders CM, McElrath TF, Scholl TO. Nutrition in adolescent pregnancy. Curr
child undernutrition: global and regional exposures and health Opin Pediatr. 2000;12(3):291–6.
consequences. Lancet. 2008;371(9608):243–60. 56. Rutstein SO. Effects of preceding birth intervals on neonatal, infant and
32. Stata: Release 13. Statistical Software. College Station [http://www.stata.com/ under-five years mortality and nutritional status in developing countries:
manuals13/svy.pdf]. Accessed 15 June 2017. evidence from the demographic and health surveys. Int J Gynecol Obstet.
33. Using Datasets for Analysis [http://dhsprogram.com/data/Using-DataSets- 2005;89:S7–S24.
for-Analysis.cfm#CP_JUMP_14042]. Accessed 15 June 2017. 57. Mozumder ABMKA, Barkat-E-Khuda, Kane TT, Levin A, Ahmed S: The effect
34. République démocratique du Congo. Enquêtes à grappes à indicateurs of birth interval on malnutrition in Bangladeshi infants and young children.
multiples: MICS 2001. Kinshasa: Ministere du Plan RDC, UNICEF; 2001. J Biosoc Sci 2000, 32(3):289-300.
35. Simler KR. Nutrition mapping in Tanzania: an exploratory analysis. In: FCND 58. Gribble JN, Murray NJ, Menotti EP. Reconsidering childhood undernutrition:
discussion paper 204. Washington, DC: International Food Policy Research can birth spacing make a difference? An analysis of the 2002-2003 el
Institute; 2006. Salvador National Family Health Survey. Matern Child Nutr. 2009;5(1):49–63.
36. Mohsena M, Goto R, NCG M-T. Regional variation in maternal and 59. Dewey KG, Cohen RJ. Does birth spacing affect maternal or child nutritional
childhood undernutrition in Bangladesh: evidence from demographic and status? A systematic literature review. Matern Child Nutr. 2007;3(3):151–73.
health surveys. WHO South East Asia J Public Health. 2015;4(2):139–49. 60. Ozaltin E, Hill K, Subramanian SV. Association of Maternal Stature with
37. République Démocratique du Congo. Enquête Démographique et de Santé Offspring Mortality, underweight, and stunting in low- to middle-income
République Démocratique du Congo 2007. Kinshasa: Ministère du Plan avec countries. Jama J Am Med Assoc. 2010;303(15):1507–16.
la collaboration du Ministère de la Santé; 2007. 61. Hernandez-Diaz S, Peterson KE, Dixit S, Hernandez B, Parra S, Barquera S,
38. République démocratique du Congo. Enquêtes à grappes à indicateurs Sepulveda J, Rivera JA. Association of maternal short stature with stunting
multiples: MICS 2010. Kinshasa: Ministere du Plan RDC, UNICEF; 2011. in Mexican children: common genes vs common environment. Eur J Clin
39. Kikafunda JK, Walker AF, Collett D, Tumwine JK. Risk factors for early Nutr. 1999;53(12):938–45.
childhood malnutrition in Uganda. Pediatrics. 1998;102(4):E45. 62. Ozaltin E, Hill K, Subramanian SV. Association of maternal stature with
40. Wu LF, Yang ZY, Yin SA, Zhu M, Gao HY. The relationship between offspring mortality, underweight, and stunting in low- to middle-income
socioeconomic development and malnutrition in children younger than countries. JAMA. 2010;303(15):1507–16.
5 years in China during the period 1990 to 2010. Asia Pac J Clin Nutr. 63. Britto RPD, Florencio TMT, Silva AAB, Sesso R, Cavalcante JC, Sawaya AL. Influence
2015;24(4):665–73. of maternal height and weight on low birth weight: a cross-sectional study in
41. Matanda DJ, Mittelmark MB, Kigaru DMD. Child undernutrition in Kenya: poor communities of northeastern Brazil. PLoS One. 2013:8(11), e80159.
trend analyses from 1993 to 2008-09. BMC Pediatr. 2014;14:5. 64. Gayle HD, Dibley MJ, Marks JS, Trowbridge FL. Malnutrition in the 1st 2
years of life - the contribution of low-birth-weight to population estimates
42. Fotso JC. Child health inequities in developing countries: differences across
in the United-States. Am J Dis Child. 1987;141(5):531–4.
urban and rural areas. Int J Equity Health. 2006;5:9.
65. Fink G, Gunther I, Hill K. The effect of water and sanitation on child health:
43. Fotso JC. Urban-rural differentials in child malnutrition: trends and socioeconomic
evidence from the demographic and health surveys 1986-2007. Int J
correlates in sub-Saharan Africa. Health Place. 2007;13(1):205–23.
Epidemiol. 2011;40(5):1196–204.
44. Smith LC, Ruel MT, Ndiaye A. Why is child malnutrition lower in urban
66. Spears D, Ghosh A, Cumming O. Open defecation and childhood stunting
than in rural areas? Evidence from 36 developing countries. World Dev.
in India: an ecological analysis of new data from 112 districts. PLoS One.
2005;33(8):1285–305.
2013;8(9):e73784.
45. Aguayo VM, Nair R, Badgaiyan N, Krishna V. Determinants of stunting and
67. Rah JH, Cronin AA, Badgaiyan B, Aguayo VM, Coates S, Ahmed S.
poor linear growth in children under 2 years of age in India: an in-depth
Household sanitation and personal hygiene practices are associated with
analysis of Maharashtra's comprehensive nutrition survey. Matern Child Nutr.
child stunting in rural India: a cross-sectional analysis of surveys. BMJ
2016;12(Suppl 1):121–40.
Open. 2015;5(2):e005180.
46. Ruel MT, Habicht JP, Pinstrupandersen P, Grohn Y. The mediating effect of
68. Fosu-Brefo R, Arthur E. Effect of timely initiation of breastfeeding on child
maternal nutrition knowledge on the association between maternal
health in Ghana. Heal Econ Rev. 2015;5:8.
schooling and child nutritional-status in Lesotho. Am J Epidemiol. 1992;
69. Patil CL, Turab A, Ambikapathi R, Nesamvuni C, Chandyo RK, Bose A, Islam
135(8):904–14.
MM, Ahmed AM, Olortegui MP, de Moraes ML, et al. Early interruption of
47. Wachs TD, Creed-Kanashiro H, Cueto S, Jacoby E. Maternal education
exclusive breastfeeding: results from the eight-country MAL-ED study. J
and intelligence predict offspring diet and nutritional status. J Nutr.
Health Popul Nutr. 2015;34:10.
2005;135(9):2179–86.
70. Kuchenbecker J, Jordan I, Reinbott A, Herrmann J, Jeremias T, Kennedy G,
48. Boyle MH, Racine Y, Georgiades K, Snelling D, Hong SJ, Omariba W, Hurley Muehlhoff E, Mtimuni B, Krawinkel MB. Exclusive breastfeeding and its effect
P, Rao-Melacini P. The influence of economic development level, household
on growth of Malawian infants: results from a cross-sectional study. Paediatr
wealth and maternal education on child health in the developing world.
Int Child H. 2015;35(1):14–23.
Soc Sci Med. 2006;63(8):2242–54.
71. Politique nationale de nutrition [http://www.pronanut-rdc.org/qui-sommes-
49. Abuya BA, Ciera J, Kimani-Murage E. Effect of mother's education on child's nous/2014-11-28-15-50-43.html]. Accessed 18 June 2017.
nutritional status in the slums of Nairobi. BMC Pediatr. 2012;12:80.
50. Makoka D, Masibo PK. Is there a threshold level of maternal education
sufficient to reduce child undernutrition? Evidence from Malawi, Tanzania
and Zimbabwe. BMC Pediatr. 2015;15:96.
51. Fall CHD, Sachdev HS, Osmond C, Restrepo-Mendez MC, Victora C, Martorell
R, Stein AD, Sinha S, Tandon N, Adair L, et al. Association between maternal
 Reproduced with permission of copyright owner.
Further reproduction prohibited without permission.