Child-Owned Poultry Intervention Effects on Hemoglobin, Anemia, Concurrent Anemia and Stunting, and Morbidity Status of Young Children in Southern Ethiopia: A Cluster Randomized Controlled Community Trial

Abstract

Cereal-based diets contribute to anemia in Ethiopian children. Eggs have nutrients to boost hemoglobin levels as well as counter concurrent anemia and stunting (CAS) and morbidity status. A community trial, targeting 6-18 months old children, was conducted in Halaba. Two clusters were randomly selected and allocated to intervention (N = 122) and control (N = 121) arms. Intervention group (IG) children received egg-laying hens with caging in a cultural ceremony declaring child ownership of the chickens. Parents promised to feed eggs to the child. Health and agriculture extension workers promoted egg feeding, poultry husbandry, and sanitation to IG families. Control group (CG) had standard health and agriculture education. At baseline, groups were not different by hemoglobin, anemia, CAS, and morbidity status. Mean hemoglobin was 11.0 mg/dl and anemia prevalence was 41.6%. About 11.9% of children had CAS and 52.3% were sick. Using generalized estimating equations, the intervention increased hemoglobin by 0.53 g/dL (ß:0.53; p < 0.001; 95% CI: 0.28-0.79). IG children were 64% (p < 0.001; odds ratio [OR]:0.36; 95% CI: 0.24-0.54) and 57% (p = 0.007; OR: 0.43; 95% CI: 0.21-0.73) less likely to be anemic and have CAS, respectively, than CG, with no difference in morbidity. Child-owned poultry intervention is recommended in settings where anemia is high and animal-source food intake is low.

Full text

Citation: Omer, A.; Hailu, D.;
Whiting, S.J. Child-Owned Poultry
Intervention Effects on Hemoglobin,
Anemia, Concurrent Anemia and
Stunting, and Morbidity Status of
Young Children in Southern Ethiopia:
A Cluster Randomized Controlled
Community Trial. Int. J. Environ. Res.
Public Health 2023,20, 5406. https://
doi.org/10.3390/ijerph20075406
Academic Editor: Paulo Santos
Received: 31 December 2022
Revised: 26 March 2023
Accepted: 29 March 2023
Published: 5 April 2023
Copyright: © 2023 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).
International Journal of
Environmental Research
and Public Health
Article
Child-Owned Poultry Intervention Effects on Hemoglobin,
Anemia, Concurrent Anemia and Stunting, and Morbidity
Status of Young Children in Southern Ethiopia: A Cluster
Randomized Controlled Community Trial
Anteneh Omer 1, * , Dejene Hailu 2and Susan Joyce Whiting 3, *
1School of Human Nutrition and Food Science, Hawassa University, Hawassa P.O. Box 5, Ethiopia
2School of Public Health, Hawassa University, Hawassa P.O. Box 5, Ethiopia
3College of Pharmacy and Nutrition, University of Saskatchewan, Saskatoon, SK S7N 5E5, Canada
*Correspondence: antenehomer@outlook.com (A.O.); susan.whiting@usask.ca (S.J.W.)
Abstract:
Cereal-based diets contribute to anemia in Ethiopian children. Eggs have nutrients to boost
hemoglobin levels as well as counter concurrent anemia and stunting (CAS) and morbidity status. A
community trial, targeting 6–18 months old children, was conducted in Halaba. Two clusters were
randomly selected and allocated to intervention (N = 122) and control (N = 121) arms. Intervention
group (IG) children received egg-laying hens with caging in a cultural ceremony declaring child
ownership of the chickens. Parents promised to feed eggs to the child. Health and agriculture
extension workers promoted egg feeding, poultry husbandry, and sanitation to IG families. Control
group (CG) had standard health and agriculture education. At baseline, groups were not different
by hemoglobin, anemia, CAS, and morbidity status. Mean hemoglobin was 11.0 mg/dl and anemia
prevalence was 41.6%. About 11.9% of children had CAS and 52.3% were sick. Using generalized
estimating equations, the intervention increased hemoglobin by 0.53 g/dL (ß:0.53; p< 0.001; 95%
CI: 0.28–0.79). IG children were 64% (p< 0.001; odds ratio [OR]:0.36; 95% CI: 0.24–0.54) and 57%
(
p= 0.007
; OR: 0.43; 95% CI: 0.21–0.73) less likely to be anemic and have CAS, respectively, than CG,
with no difference in morbidity. Child-owned poultry intervention is recommended in settings where
anemia is high and animal-source food intake is low.
Keywords: egg; poultry; hemoglobin; anemia; concurrent anemia and stunting; morbidity
1. Introduction
Anemia remains a global public health challenge, affecting about 40% of children
6–59
months old [
1
]. Anemia has multifaceted causes, ranging from acute blood loss, nutri-
ent deficiencies and infection, to autoimmune and genetic disorders. Nutrient deficiency
and inflammation are the most common causes of anemia in children [
2
]. Among nutrients,
particularly iron, vitamin B12, vitamin A, folate, zinc and protein deficiencies are associated
with anemia [
2
–
4
]. Unfortunately, the diets of children under two of age in Africa and
South Asia usually lack or poorly provide these nutrients [
5
,
6
]. Children in Africa, East
Asia, and the Pacific and South Asia rank the highest in one or more of the deficiencies of
iron, zinc, and vitamin A [7].
The most recent Ethiopian demographic and health survey (EDHS) reported that more
than half of children below 5 years of age were anemic and, opposite to the global trend,
the prevalence of anemia had increased compared to the preceding EDHS survey [
8
]. In
Ethiopia, iron deficiency accounts for 25–36% of total anemia among pre-school children [
9
].
A recent study attributed iron deficiency and inflammation to cause 21% and 5% of total
anemia among 6–59 months old children, respectively [
10
]. The cause of the remaining
portion of anemia is not well-defined. Ethiopia set a target of decreasing anemia to 40% by
the year 2025 [11].
Int. J. Environ. Res. Public Health 2023,20, 5406. https://doi.org/10.3390/ijerph20075406 https://www.mdpi.com/journal/ijerph

Int. J. Environ. Res. Public Health 2023,20, 5406 2 of 16
The usual diets of children 6–24 months old in Ethiopia are cereal-based, rarely con-
taining animal-source foods. Studies reported that, except for iron, dietary intakes of
zinc, folate, vitamin B12, vitamin A, and protein among Ethiopian children are generally
inadequate [
9
,
10
,
12
]. Due to the poor protein and micronutrient content of complemen-
tary foods, high demand for nutrients and frequent episodes of diseases together with
environmental and other factors, under two years of age children are the most vulnerable
group to anemia and its far-reaching consequences [
2
]. Anemia greatly impairs the immune
system, thus increasing the risk of morbidity and mortality among young children. It
also impairs neuro-cognitive and motor development hampering school performance and
productivity [2].
Nutrition interventions have had encouraging results in alleviating anemia among
infants and young children. Home fortification of children’s diet using micronutrient
sprinkles [
13
–
15
] and lipid-based nutrient supplements [
16
–
19
] are well-documented strate-
gies of anemia reduction, improvement of iron status, and hemoglobin levels. Nutrition
education that improved infant feeding practices significantly decreased anemia and in-
creased hemoglobin compared with the existing intervention [
20
] and WASH/Malaria
intervention [21].
Reports from food-based strategies are inconsistent. Caterpillar cereal compared with
the usual diet in Democratic Republic of Congo increased hemoglobin significantly [
22
].
Locally produced food products containing germinated amaranth, maize, small fish, and
edible termites in Kenya decreased hemoglobin and iron status [
23
] compared with corn-
soy blend (CSB), most likely due to the iron bioavailability inhibition effect of the amaranth.
Rice-based complementary foods with small fish and edible spiders in Cambodia com-
pared with CSB showed no effect on iron status [
24
]. A trial that compared meat with
multi-micronutrient-fortified rice-soy cereal reported no difference in anemia rates but
significantly lowered the iron deficiency among the cereal group [
25
]. After providing one
egg daily for six months in Malawi, no difference was found with the control group (no egg)
in the prevalence of anemia, iron deficiency and iron deficiency anemia, hemoglobin levels,
and iron status [
26
]. Little research has been done in Ethiopia on the effects of nutrition
interventions on anemia among infants and young children.
We recently implemented a nutrition-sensitive child-owned poultry intervention that
provided chickens and caging materials, declaring ownership to the children with the aim
of increasing egg intake and minimizing disease risk from direct contact with the birds
and their feces. Poultry husbandry was improved, and egg intake was increased in the
intervention group (mean weekly egg intake 4.85 vs. 0.4; p< 0.001) [
27
]. In addition, at
six months, underweight and stunting reduced; weight for age and weight for height
z-scores increased and motor skills (running, kicking ball, and throwing ball milestones)
were attained at an earlier age significantly compared to the control group [28].
Our pilot study conducted in 2016 recorded a marginally significant reduction of
anemia (RR = 0.48; 95% CI = 0.24–0.96) after providing a gift of egg-laying hens to children
and promoting separate chicken sheltering [
29
]. Although awareness of disease risk related
to chicken production was enhanced and the practice of keeping chickens separately
improved significantly compared to the baseline and control group, only a quarter of
intervention households were able to have and utilize cages. Due to economic reasons,
most cages were made from farm leftover stalks of maize and sorghum that were not strong
enough to last long [
30
]. Observational studies in Sub-Sahara Africa associated livestock
ownership including poultry with anemia and lower hemoglobin [
31
,
32
] although this
was not always the case [
33
]. Taking the challenges related to the construction of separate
chicken shelters observed in the pilot study and the probable negative effect of rearing
chickens on child health and nutrition outcomes including masking of intervention effects
into consideration, this project provided cages beside chickens to minimize the disease risk
from direct contact with the birds and their feces. This paper reports on the intervention
effects on hemoglobin, anemia, and morbidity status of young children.

Int. J. Environ. Res. Public Health 2023,20, 5406 3 of 16
2. Materials and Methods
2.1. Study Design, Participants, and Sample Size
With a 6-months follow-up period, a cluster randomized and controlled community
trial (Trial registration: NCT 03355222) was conducted from May to November 2018 in
Halaba district, Southern Nations Nationalities and Peoples Region (SNNPR), 85 km
southwest of Hawassa, the regional capital. Halaba is classified as midland with an average
elevation of 1800 m above sea level. Livelihood mainly depends on rainfed farming mixed
with livestock production. Maize, sorghum, teff, haricot bean, wheat, millet, and chili are
the major agricultural products of the district. Due to erratic and irregular rainfall, Halaba
is frequently affected by drought and is endemic to malaria. [
34
]. The district is divided
into 10 catchments (clusters), each having 1 health center that oversees health posts that
function in kebeles/villages inside the catchment. Health Extension Workers (HEWs) based
in health posts provide health and nutrition services to the community with the support of
Health Development Team Leaders (HDTLs) who are volunteers networking at a ratio of 1
for every 30 households.
From the 10 clusters in the district, 2 were randomly selected and allocated to interven-
tion and control wings. For matching reasons, a kebele/village was purposely chosen from
each selected cluster. Distance from their respective catchment health center and existing
health, nutrition, and agriculture interventions were taken into consideration during village
selection. The kebeles selected for the study do not have a common marketplace. In addi-
tion, they are located in opposite directions (east and west) to the district administrative
center, Halaba Kulito town.
The study was powered to observe the effect of the intervention on hemoglobin levels.
We did not find trials that assessed the effect of egg intake on hemoglobin among under
two years old children except for one, which evaluated the consumption of four egg yolks
per week (excluding the egg white) and recorded no significant effect on hemoglobin [
35
].
Hence, a medium effect size (0.5) was entered in the calculation with a design effect
of 2, power of 80%, and 10% loss to follow-up, which provided a sample size of 126
mother-child dyads for each study group. After excluding those who were sick and taking
drugs, on nutritional treatment or severely and acutely malnourished, and reported by
their caregivers to be allergic to eggs, a total of 253 apparently healthy 6–18 months old
children who lived for at least 6 months in the selected kebeles were enrolled in the study
(Intervention Group, IG, [N] = 127, Control Group, CG, [N] = 126). Detailed information on
sampling, participants’ enrolment, and study protocol has been published [27].
Participant families, HEWs, HDTLs, and agriculture extension workers (AEWs) in
both study villages were not informed about the existence of the two study groups. Data
collectors deployed for baseline and end line surveys were different and not informed
regarding the allocation of study groups. Medical laboratory technologists who collected
samples as well as carried out lab analysis were not aware of any study groups. Samples
sent to the laboratory for analysis were uniquely coded with no identifiable information
about where they came from and the name of the subject.
2.2. Intervention
The intervention had three core components: local capacity building, chicken and
caging gift, and social and behavior change communications (SBCC), and these have been
previously described in detail [
27
]. In brief, HEWs, AEWs, and HDTLs, who were frontline
implementers at the kebele level, received two days of training on the benefits of egg
consumption for children’s health and nutrition, the risk of disease transmission from free-
range chickens and its related possible negative effects, the importance of cage utilization
and environmental sanitation and improved poultry husbandry, and their role in the study.
Workers in the control kebele received the usual nutrition and agriculture training provided
to them with their position.
Following the capacity-building training, religious leaders, community elders, and
village management team in the intervention kebele were sensitized about the objective

Int. J. Environ. Res. Public Health 2023,20, 5406 4 of 16
and approach of the research project and their role in the study, paving the way to the
implementation of Chicken and Caging Gift Ceremony (CCGC). The CCGC is an innovative
community-based culture and religion-sensitive approach that empowers children to be
owners of chickens and the eggs that they produce, aiming for one-egg-a-day consumption.
AEWs organized the gift ceremony in collaboration with HEWs and HDTLs in the kebele
farmer’s training center (FTC). Religious leaders declared ownership of the chickens and all
the eggs they would produce to the children and marked the practice of selling or sharing
the eggs with anyone or the chickens as “Haram”, an Arabic term meaning forbidden.
Families promised to add at least two more hens, replace them if the birds die, not to
sell or share the eggs and to feed the chicken-owner child one egg a day. Parents signed
and received two egg-laying local breed hens, vaccinated for Newcastle disease, on behalf
of the children. Two types of cages were also provided. One was a night coop that is
locally made, lightweight to move around, easily cleanable, and can accommodate up to
eight chickens. The other cage was an enclosure (25 square meter) where the chickens
spend the day roaming for food and rest. Wood logs, mesh wire, and nails were provided,
and families built the cage in their own compounds after learning how to by creating a
model with AEWs at the kebele FTC. The AEWs also provided orientation on utilizing and
cleaning the night coop.
After the gifting of chickens and caging was done, HEWs held a demonstration of
two types of egg preparations at the health post: hard-boiled and smashed egg yolk for
children 6–7 months old and boiled and smashed whole egg for children above 7 months.
Following HEWs’ instructions, caregivers boiled and smashed the egg (egg yolk or whole
egg depending on their child’s age), expressed breast milk to soften the preparation for
easy swallowing and fed their children during the session.
Having dietary, anthropometry and child-owned poultry production assessment
findings, the HEWs and AEWs provided tailored individual counselling every month
using SBCC cards prepared for this purpose based on their area of specialty. In their
counselling, they promoted one egg-a-day consumption, child-owned poultry production,
cage utilization, improved poultry husbandry, and environmental sanitation. HDTLs also
passed the SBCC messages to the households under their network. Any contact with
caregivers including monthly data collection, home visits, and caregivers’ visits to the
health post for health service was used as an opportunity to promote baby-friendly chicken
production and egg feeding.
2.3. Ethics Approval
The study was approved by Hawassa University, Ethiopia, and the University of
Saskatchewan, Canada. Formal communication was made with district and kebele-level
health, agriculture, and administration offices. Consent was obtained from all caregivers to
participate in the study. They were also informed of lab tests and procedures before sample
collection. They received a bar of soap and oil as compensation for their time during the
follow-up. Children excluded from the study due to reports of egg allergy were equally
treated by being rewarded with chickens like the participant children. Children in the
control group also received egg-laying hens along with CCGC messages but only after the
end line survey.
2.4. Measurements
Baseline information was collected on sociodemographic and economic characteristics,
infants and young child feeding practices, livestock production, and poultry husbandry
practices. The intervention effect on hemoglobin and anemia status was the primary
outcome of this study, while morbidity status was measured as a secondary outcome.
Effects on child-owned poultry production, egg intake, anthropometry, and gross motor
skills development were reported previously [27,28].
Two medical laboratory technologists measured hemoglobin concentration using a
portable spectrophotometer (Hemocue Hb 301; HemoCue AB, Ängelholm, Sweden) and

Int. J. Environ. Res. Public Health 2023,20, 5406 5 of 16
the presence of antigens of P. falciparum and P. vivax using rapid diagnostic test CareStart
™
Malaria HRP2/pLDH (Pf/Pv) Combo, Kit/25 (Access Bio Inc., Addis Ababa, Ethiopia) at
baseline and end line. Tests were carried out in the field from finger-prick blood samples
following the manufacturer’s instructions.
Formol-ether concentration technique was run to test intestinal helminthiasis from
randomly selected sub-samples (50 children) from each group following standard operating
procedures presented by Cheesbrough [
36
]. Stool samples were transported to Halaba
General Hospital Laboratory Parasitology Unit for analysis after being emulsified in 10%
formol water. At the laboratory, the formol-fecal suspension was strained first, 10% formol
water was added, and it was centrifuged for 1 min. To the sediment, 8 mL of formol water
and 4 mL of diethyl ether were added and centrifuged. Then, the sediment was examined
under a microscope for intestinal helminths with egg count.
Morbidity symptoms of fever, coughing, vomiting, and diarrhea as well as skin,
eye, and ear infections that occurred in the last two weeks before the date of assessment
were recorded at baseline and monthly during follow-up based on caregivers’ reports.
Diarrhea was defined as the passage of three or more loose or liquid stools per day (or
more frequent passage than is normal for the individual) [
37
]. Caregivers were informed
to report vomiting when their child forcefully threw up food; not spit out small amounts
of food. Fever was defined as hot to the touch. A child was recorded to have a cough if
the cough, regardless of the duration, came with one of these symptoms: a runny nose or
cold, trouble breathing, fever (hot to touch), wheezing sound, and being constant (several
times in a day) or stayed for more than two days with no additional symptoms [
38
]. The
presence of one of these symptoms was reported as a skin infection: itching rash with
small papules, visible lesions, fluid-filled vesicles and blisters, abscess, ringworm (itchy
circular lesion with a fine scaly area on body and scalp), and scabies [
39
]. Indications of
ear infection included the presence of pus draining from one or both of the ears or the
child being irritable and rubbing his/her ear [
40
]. Eye infection/disease was defined as
having one of these symptoms: discharge from the eyes; eyelids that are stuck together
after waking from sleep; red eyes/eyelids and swollen eyelids; visible white or gray sore
on the iris; white foamy lesions on the conjunctiva [41,42].
2.5. Data Analysis
Hemoglobin values were adjusted for altitude before analysis as per WHO guide-
line [
43
]. Baseline characteristics were presented with descriptive analysis and comparisons
between groups were made by chi-square and independent samples t-test for categorical
and continuous variables, respectively. Considering the cluster randomization design of
the study and some missed subjects during follow-up, the Generalized Estimating Equa-
tions (GEE) model was primarily utilized to evaluate intervention effects on hemoglobin
levels and status of anemia, concurrent anemia and stunting (CAS), and morbidity. GEE
of linear and binary logit models was run for continuous and categorical variables, re-
spectively. Stratified analysis was also conducted to evaluate intervention effects among
specific groups. Effect sizes were reported as beta (
β
), odds ratio (OR), and relative risk
(RR). p-values < 0.05 were taken as statistically significant. Data were processed using IBM
SPSS version 28 (Chicago, IL, USA).
3. Results
A total of 243 children completed the study and entered into the analysis. It was
necessary to exclude seven children who were lost to follow-up and three children who
were found to be sensitive to eggs. A flow diagram has been previously published [27].
3.1. Baseline Characteristics
Except for child sex (X
2
= 8.77; p= 0.003), socio-economic and demographic char-
acteristics including poultry production and husbandry, infant and young child feeding
practices and maternal characteristics were not significantly different among the study

Int. J. Environ. Res. Public Health 2023,20, 5406 6 of 16
groups (Table 1). Detailed information has been previously published [
28
]. Groups were
also comparable at enrollment by their nutritional, malaria, intestinal helminthiasis, total
anemia, and morbidity status.
Table 1. Selected baseline characteristics and IYCF practices.
Description Intervention (N = 127) Control (N = 126)
N % N %
Livestock production
Poultry production Chicken 26 20.5 33 26.2
Chicken care Day cage/separated place a3 11.5 2 6.1
Night shelter/cage a5 19.2 5 15.2
Maternal Characteristics
Age in years Mean age (SD) 27.3 (4.68) 27.5 (4.18)
Education on feeding eggs Received 51 40.2 52 41.3
Awareness of chicken feces
as risk to child Aware 30 23.6 40 31.7
Child Characteristics
Sex Female * 46 36.2 69 54.8
Age (month) Mean (SD) 10.9 (3.18) 11.4 (4.28)
IYCF
Breastfeeding Currently fed on
breastmilk 125 98.4 122 96.8
Complementary food (CF)
Currently on CF 120 94.5 117 92.9
Mean age of introduction:
months (SD) 6.13 (0.59) 6.2 (0.69)
Egg intake history Ever fed 65 51.2 57 45.2
% children fed with egg 24 h before survey 10 7.9 12 9.5
The week before survey 30 23.6 35 27.8
Eggs consumed per week Mean (SD) 0.23 (0.42) 0.29 (0.51)
* Statistically significant (p< 0.05). IYCF = infant and young child feeding.
a
Computed among chicken owners
(denominator is 26 for intervention and 33 fir control group).
3.2. Intestinal Helminthiasis and Malaria Infection
No child was positive for intestinal helminth at baseline and malaria at baseline and
end line in both groups. About 7% of the children had helminth infection at end line with
no group difference (p= 0.436). Except for one child who was diagnosed with Ascaris
lumbricoides (220 eggs/gram of feces), the others were infected with Hymenolepis nana
(egg count ranging from 2 to 19 eggs/gram of feces). No multiple helminth infections
were found.
3.3. Hemoglobin, Anemia, and Concurrent Anemia and Stunting (CAS)
Among the total children, mean hemoglobin concentration at baseline was 11.0 g/dL.
Anemia prevalence was 41.6% of which mild, moderate, and severe anemia constituted
61.4%, 36.6%, and 2%, respectively. About 11.9% of the children were both anemic and
stunted (CAS). Mild anemia was more prevalent in the intervention group (X
2
= 4.063;
p= 0.044) as moderate anemia was in the control (X2= 2.654; p= 0.103). GEE showed that
hemoglobin was significantly increased by 0.53 among intervention children compared
to the control at the end line (Table 2) after adjusting for baseline weight for age z-scores.
Child age and sex did not modify the effect on hemoglobin. The mean hemoglobin level

Int. J. Environ. Res. Public Health 2023,20, 5406 7 of 16
among children in the control group declined at six months, which was accompanied
by significantly increased anemia and CAS prevalence. On the contrary, children in the
intervention group were 64% and 57% less likely to be anemic and concurrently affected by
anemia and stunting, respectively, compared to children in the control.
Table 2. Intervention effect on hemoglobin, anemia, and concurrent anemia and stunting (CAS).
Baseline End Line Unadjusted Adjusted
IG
(N = 122)
CG
(N = 121)
IG
(N = 122)
CG
(N = 121) Effect Size 1Effect Size 1
Mean (SD) Mean (SD) Mean (SD) Mean (SD) β(95% CI) apβ(95% CI) ap
Hgb 11.1 (1.1) 10.9 (1.4) 11.4 (1.0) 10.6 (1.4) 0.52 (0.26, 0.77) <0.001 0.53 (0.28, 0.79) †<0.001
N (%) N (%) N (%) N (%) OR (95% CI) bpOR (95% CI) bp
Anemia 50 (41) 51 (42.1) 26 (21.3) 70 (57.9) 0.45 (0.30, 0.68) <0.001 0.36 (0.24, 0.54) †† <0.001
CAS 16 (13.1) 13 (10.7) 8 (6.6) 29 (24) 0.52 (0.29, 0.94) 0.031 0.43 (0.23, 0.80) ††† 0.007
IG = Intervention group; CG = Control group; Hgb = Hemoglobin; CAS = Concurrent anemia and stunting;
OR = Odds
ratio. Independent, auto-regressive, and exchangeable working correlation matrices provided the
same results.
1
Computed by Generalized Estimating Equations (GEE) linear (
a
) and binary logit (
b
) models.
†
Adjusted for baseline weight for age z-scores.
††
Adjusted for baseline hemoglobin values.
†††
Adjusted for
baseline length for age, weight for age, and weight for length z-scores.
Stratified analysis showed that mean hemoglobin levels increased among children in
the intervention group at six months regardless of baseline nutritional status. Significant
increases in mean hemoglobin concentrations were observed only among children with
normal nutritional status (normal weight, not stunted, and not wasted) compared to their
matches in the control (Table 3). Underweight, stunted, and wasted children at baseline
were too few to evaluate the effect of the intervention on hemoglobin. Effect sizes found in
all strata of normal nutritional status were almost the same (
β
ranging from 0.53–0.54 and
95% CI = 0.24–0.28; 0.81–0.82). Hemoglobin concentrations improved in both intervention
and control groups at six months among children anemic at baseline, but the incremental
increase was significantly higher in the intervention arm (
β
= 0.83; 95% CI = 0.47, 1.19)
than in the control. In contrast, mean hemoglobin concentrations declined in both study
groups among children who were non-anemic at baseline; however, hemoglobin decreased
less in the intervention group than in the control. From all strata analyzed, the highest
hemoglobin increase was observed among anemic children.
Regardless of the baseline nutrition, anemia, and CAS status of the children, the
prevalence of anemia and CAS decreased at endline in the intervention group while it
increased in the control (Tables 3and 4). More than 4 out of 10 and nearly 1 out of 5 children
in the control group who had no anemia and CAS at enrollment developed anemia and
CAS, respectively, by six months. The odds of developing anemia and CAS among non-
anemic and non-CAS children at baseline was reduced by 75% and 78%, respectively, in the
intervention group compared to control. About 70% of anemic children and more than 80%
of children with CAS at enrollment in the intervention group no longer had anemia and
CAS, respectively, at 6 months. On the contrary, more than 80% and 69% of children affected
by anemia and CAS, respectively, at baseline in the control group remained classified as
anemic and having CAS at end line.

Int. J. Environ. Res. Public Health 2023,20, 5406 8 of 16
Table 3.
Intervention effect on hemoglobin and anemia among groups stratified by baseline nutrition,
anemia and CAS status.
Strata N
Hemoglobin Anemia
Baseline End Line Effect Size 1Baseline End Line Effect Size 2
Mean (SD) β
(95% CI) pN (%) OR
(95% CI) p
Normal
Weight
IG 100 11.2 (1.1) 11.4 (1.0) 0.54
(0.26, 0.81)
<0.001
39 (39.0) 21 (21.0) 0.40
(0.26, 0.64)
<0.001
CG 97 10.9 (1.3) 10.6 (1.3) 41 (42.3) 59 (60.8)
Not Stunted IG 87 11.2 (1.1) 11.4 (1.1) 0.53
(0.24, 0.82)
<0.001
34 (39.1) 19 (21.8) 0.38
(0.23, 0.62)
<0.001
CG 84 11.0 (1.1) 10.6 (1.4) 38 (45.2) 52 (61.9)
Not Wasted IG 111 11.2 (1.1) 11.4 (1.0) 0.54
(0.28, 0.81)
<0.001
44 (39.6) 23 (20.7) 0.43
(0.28, 0.65)
<0.001
CG 111 10.9 (1.4) 10.6 (1.4) 48 (43.2) 64 (57.7)
Anemic IG 50 10.1 (0.8) 11.3 (1.0) 0.83
(0.47, 1.19)
<0.001
50 (100.0) 15 (30.0) 0.11
(0.04, 0.26) a
<0.001
CG 51 9.7 (1.3) 10.1 (1.2) 51 (100.0) 41 (80.4)
Non-Anemic IG 72 11.8 (0.6) 11.5 (0.9) 0.27
(0.03, 0.51) 0.026 0 (0) 11 (15.3) 0.25
(0.12, 0.57) a0.001
CG 70 11.7 (0.6) 11.0 (1.0) 0 (0) 29 (41.4)
Non CAS IG 106 11.3 (1.0) 11.4 (1.0) 0.44
(0.20, 0.69)
<0.001
34 (32.1) 21 (19.8) 0.41
(0.26, 0.65)
<0.001
CG 108 11.4 (1.0) 10.7 (1.4) 38 (35.2) 61 (56.5)
IG = Intervention group; CG = Control group; CAS = Concurrent anemia and stunting; OR = Odds ratio.
1
Computed by GEE linear model.
2
Computed by GEE binary logit model except those denoted by (
a
) that
the odds ratio was calculated by binary logistic regression.
1,2
Working correlation matrices of independent,
auto-regressive, and exchangeable provided similar results.
Table 4.
Intervention effect on CAS among the groups stratified by baseline nutrition, anemia, and
CAS status.
Strata N
Baseline End Line
OR (95% CI) 1p
N (%)
Normal weight IG 100 11 (11) 6 (6)
0.28 (0.11, 0.74)
0.010
CG 97 5 (5.2) 18 (18.6)
Not wasted IG 111 15 (13.5) 7 (6.3)
0.22 (0.09, 0.53)
0.001
CG 111 12 (10.8) 26 (23.4)
Stunted IG 35 16 (45.7) 4 (11.4)
0.17 (0.05, 0.58)
0.005
CG 37 13 (35.1) 16 (43.2)
Not stunted IG 87 0 (0) 4 (4.6)
0.26 (0.08, 0.84)
0.025
CG 84 0 (0) 13 (15.5)
Anemic IG 50 16 (32.0) 5 (10.0)
0.20 (0.07, 0.61)
0.004
CG 51 13 (25.5) 18 (35.3)
Non-anemic IG 72 0 (0) 3 (4.2)
0.23 (0.06, 0.88)
0.031
CG 70 0 (0) 11 (15.7)
CAS IG 16 16 (100) 3 (18.8)
0.10 (0.02, 0.57)
0.010
CG 13 13 (100) 9 (69.2)
Non-CAS IG 106 0 (0) 5 (4.7)
0.22 (0.08, 0.61)
0.003
CG 108 0 (0) 20 (18.5)
IG = Intervention group; CG = Control group; CAS = Concurrent anemia and stunting; OR = Odds ratio.
1Computed by binary logistic regression.

Int. J. Environ. Res. Public Health 2023,20, 5406 9 of 16
3.4. Morbidity Symptoms
More than half of the children in both groups exhibited one or more morbidity symp-
toms at baseline that remained unchanged at six months. Groups were not different in
morbidity symptoms (fever, cough, diarrhea, and vomiting) and infections of the skin, eye,
or ear at baseline and end line. Adjusted analysis (child sex and age, baseline anemia and
nutritional status, and baseline hemoglobin levels) also did not find a significant difference
between groups at end line. However, reductions in episodes of vomiting and eye, ear
and other infections were recorded at end line in both groups (Table 5). Among the total
children, older ages were found to become sick less (showing any morbidity symptom
or skin, eye, ear, and other infection) at end line (p= 0.026;
β
=
−
0.040; 95% CI =
−
0.076,
−0.005).
Table 5.
Effect of nutrition-sensitive child-owned poultry intervention on the prevalence of morbidity
symptoms.
Morbidity
Baseline End Line
OR (95% CI) 1p
IG
(N = 122)
CG
(N = 121)
IG (N =
122)
CG
(N = 121)
%%%%
Any symptom 51.6 52.9 54.1 58.7 0.81 (0.62–1.04) 0.102
Fever 35.2 28.1 27.0 31.4 0.81 (0.61–1.08) 0.144
Cough 27.0 19.8 29.5 27.3 0.95 (0.70–1.28) 0.736
Diarrhea 18.0 14.9 20.5 17.4 0.79 (0.56–1.10) 0.158
Vomiting 16.4 14.9 6.6 9.9 0.77 (0.52–1.17) 0.220
Skin Infection 7.4 4.1 7.4 6.6 1.10 (0.66–1.86) 0.709
Eye, ear and other infections 9.8 12.4 1.6 4.1 1.27 (0.72–2.23) 0.413
1Computed by GEE binary logit model with exchangeable correlation matrix. Independent and auto-regressive
correlations provided very close results to exchangeable matrix. No significant difference was found among
groups in all working correlations matrices.
4. Discussion
Our innovative nutrition-sensitive poultry intervention that enabled children to be
owners of chickens improved hemoglobin concentrations and reduced the prevalence of
anemia and concurrent anemia and stunting at six months. The intervention has resulted in
significantly improved poultry husbandry practices, particularly cage utilization, increased
egg intake and improved nutritional status and attainment of developmental milestones,
which has been published previously [27,28].
The mean hemoglobin of the children was higher and anemia prevalence was lower
at baseline than that of children under two years old who participated in the 2016 EDHS:
Hgb = 10
±
1.63 g/dL; anemia prevalence of 71.9% [
44
]. The baseline anemia prevalence
was comparable with what was found among 6–23 months old children who lived in
rural Ethiopia in the midland agroecology [
45
]. Our intervention increased hemoglobin by
0.53 g/dL, unlike the egg trial in Malawi, which provided eggs to 6–9 months old children
for daily consumption (Mazira project) and reported no improvement in hemoglobin
concentration, ferritin, soluble transferrin receptor, and body iron index. No difference was
also seen among egg and no egg groups in anemia, iron deficiency, and iron deficiency
anemia prevalence [
26
]. The high burden of iron deficiency at enrolment and sustained
inflammation during the study period was presented as the reason why egg intake could
not improve the iron and anemia status of the children. In addition, the inhibition effect of
phosvitin and ovotransferrin found in the egg yolk on nonheme iron from other foods and
the high fish intake in both groups might have also hampered the intervention effect [46].
It is important to note the context difference between the Mazira project and our
project. In the Mazira children, iron deficiency is found concurrently with 93% of the

Int. J. Environ. Res. Public Health 2023,20, 5406 10 of 16
anemia and more than 98% to 100% prevalence of iron intake inadequacy was recorded
at midline and end line [
26
,
47
]. Although we did not measure iron status, children in
our project had higher hemoglobin levels and lower anemia prevalence than the Mazira
children at baseline; most likely indicating better iron status. Another important difference
to note is that children in the Mazira project had adequate baseline protein intake from
complementary foods, including fish and breast milk [
47
]. About 32.8%, 8.7%, and 5.5% of
children in our study had cow milk, egg, and legumes and nut intake, respectively, and
no child had an intake of flesh foods on the day before the baseline survey. Moreover, the
inhibition effect of egg yolk proteins might be minimum or nil in our study as caregivers
were trained to feed the egg on its own, although they were free to prepare the egg in
boiled or fried form as long as it was cooked well. Feeding eggs mixed with other foods
was not reported at all during monthly counselling as well as home visits. In our pilot
study, mixing eggs with other foods (mostly boiled and smashed potato) was reported by
caregivers as a remedial action when they felt their child was sensitive to eggs [29]. Three
children were found to be sensitive to eggs in the current study and we excluded them
from the analysis of intervention effect on health and nutrition status.
Recent evidence revealed that iron deficiency accounted for 21% of anemia while folate
and infection accounted for 6% and 5%, respectively, among the under-five population of
Ethiopia [
10
]. Gashu et al. (2016) reported a very low prevalence of iron deficiency (9.1%)
and iron deficiency anemia (5.3%) among children consuming a predominantly unrefined
plant-based diet [
48
]. Cereals in Ethiopia have high iron content [
49
] and provide adequate
iron, even under the assumption of low bioavailability (5%) [
50
]. This is partially due to
extrinsic iron from soil contamination during harvesting and threshing of the grains [
51
,
52
]
combined with the fermentation process during food preparation, which increases the
bioavailability [53,54].
However, protein and micronutrient intakes, particularly vitamin A, zinc, folate, and
vitamin B12, are very low [
10
,
12
]. Nearly two-thirds of children under five years old in
Ethiopia’s southern region have inadequate protein intake, which is the lowest compared
to the other regions [
12
]. The Ethiopia national food consumption survey also reported that
the inadequacy of protein intake was associated with low consumption of flesh foods and
legumes, and having an intake of foods that were poor in protein content and amino acid
composition. This is in agreement with our dietary intake findings. Based on the existing
evidence, micronutrients (other than iron), and protein deficiencies are important causes of
nutritional anemia among Ethiopian children.
Protein intake has been associated with improved hemoglobin status. Valine, leucine,
and isoleucine (branched chain amino acids (BCAA)) were reported to be positively and
significantly correlated with levels of hemoglobin and anemic individuals were found
to have significantly lower serum BCAA concentrations than non-anemic ones [
55
]. Pro-
tein deficiency is associated with reduced iron incorporation into hemoglobin [
56
], and
low consumption of protein-source foods was associated with iron deficiency anemia in
Ethiopia [
57
]. Improved amino acid intake increases hematopoiesis [
58
]. Egg white protein,
particularly ovalbumin, has significant benefits in recovery from iron deficiency anemia
in animal models [
59
]. Egg consumption substantially contributes to dietary adequacy
of protein, fat, pantothenic acid [
47
,
60
–
63
], energy [
64
], phosphorus, vitamin D [
61
–
63
],
vitamin B12 [
47
,
61
], biotin, vitamin E, cholesterol [
61
], choline, and its metabolites including
docosahexaenoic acid (DHA) [
62
,
63
,
65
], riboflavin, selenium, vitamin A [
47
,
62
],
α
-linolenic
acid, lutein + zeaxanthin, and potassium [
62
]. Provided that iron intake is adequate in
our context, despite the source, we deemed that the increased egg intake improved the
protein and micronutrient status of the children, which ultimately increased hemoglobin
concentrations and reduced anemia and CAS prevalence [
27
]. We previously showed that
the effect of whole egg intake was also observed in improving the nutritional status and
motor development of the children [28].
The magnitude of CAS in this study population at baseline (11.9%) was lower than the
national CAS rate among 6–23 months (23.9%) [
66
]. However, CAS rate in the control group

Int. J. Environ. Res. Public Health 2023,20, 5406 11 of 16
reached the national level at end line (24%). Comparable prevalence (25.3%) was recorded
among 6–23 months children in two districts from north and south Ethiopia [
45
] and
pooled proportion of CAS among 6–59 months from 43 low and middle-income countries
(21.5%) [
67
]. The study area and age difference might be the reason for the lower CAS
prevalence at enrollment in our study population. CAS prevalence decreased significantly
in the intervention group at six months. This might be due to the increased protein and
micronutrient intake from the eggs as well as the consumption of vitamin A-rich fruit and
vegetable intake, which significantly increased in the intervention group as a result of sales
of excess eggs [
27
]. Analysis of the 2016 DHS data revealed that increased protein intake
and consumption of vitamin A-rich fruit and vegetable intake were associated with lower
odds of CAS in Ethiopia [66].
Although anemia and stunting are two different body conditions, they have communal
determinants and pathways that are important to consider when designing interventions.
Undernutrition causes both anemia and stunting as infection exacerbates both condi-
tions
[2,68]
. Age and sex [
66
,
69
,
70
], low dietary diversity [
70
–
72
], not achieving minimum
meal frequency [
45
], multiple micronutrient deficiencies [
73
], rural residence, and low
household wealth (living in poorer households) [
66
,
67
,
69
], infection [
66
,
69
], drinking un-
safe water [
70
,
71
], and household food insecurity [
70
,
72
,
74
] are important determinants of
both stunting and anemia. Anemia and stunting are strongly associated with each other [
75
].
Stunted children have a higher risk of anemia than non-stunted ones and vice versa [
76
].
Stunting is a predictor of anemia [
45
,
72
,
77
] and vice versa [
71
,
78
]. Thus, interventions that
improved the determinants or the causes communal to stunting and anemia might be effec-
tive in reducing CAS, as observed in our nutrition-sensitive child-owned poultry project
that improved dietary diversity, macro-and micronutrient intake, and nutritional status.
Livestock ownership, such as sheep and goats, was significantly and positively as-
sociated with child anemia in Ghana, while free-range poultry showed marginal signifi-
cance [
32
]. In Ghana, using population data, the household ownership of chickens, but not
other animal species, was associated with higher odds of anemia among under-five years
old children [
31
]. A systematic review reported that poultry production interventions, in
contrast to observational studies, had modest benefits on anemia [
79
]. Chicken ownership
was not associated with lower hemoglobin concentrations among children in Sub-Saharan
Africa [
80
]. A recent study in Ghana found lower odds of anemia among children from
households owning cattle, small livestock (goats, sheep, or pigs), and poultry than those
owning no livestock [
33
]. We reported a marginally significant reduction of anemia in our
pilot project [
29
] in which less than 6% of intervention households used separate chicken
shelters at baseline, which increased to 25% at 6 months [
30
]. In the current study, we found
a very significant reduction of anemia and CAS and increased hemoglobin concentrations
with much bigger effect sizes. Besides increased egg intake, the improved poultry hus-
bandry practice particularly cage utilization might have contributed to this result. Almost
all households in the intervention group utilized cages and kept chickens separately day
and night throughout the study period [
27
], which might have minimized the contact of
the children with the birds and their feces, although we did not measure this variable.
Campylobacter infection transmitted from poultry is associated with environmental enteric
dysfunction, a chronic sub-clinical condition that causes loss of nutrients by inhibiting ab-
sorption and leaking out nutrients [
81
]. While a study in Ethiopia found no harmful effects
of the provision of chickens on child anemia [
82
], it is recommended to use cages to keep
chickens away from children and minimize fecal contamination of the home environment.
The child-owned poultry intervention showed no significant effect on reducing mor-
bidity symptoms. Our pilot study [
29
] and the Ecuador egg trial [
83
] also did not find an
effect on the reduction of morbidity symptoms. Vomiting was seen more frequently in
the pilot study treatment group, which might be due to egg sensitivity. About 7.5% of the
children (n= 18) in the intervention group had developed egg sensitivity. In the current
study, only three children were found to be sensitive to egg. The Ecuador trial [
83
] recorded
diarrhea reports more in the egg group, which might have been related to egg intake, which

Int. J. Environ. Res. Public Health 2023,20, 5406 12 of 16
is not the case in this study as diarrhea almost equally increased in both groups at end
line. The absence of increased prevalence of morbidity symptoms and the improvements
observed in the reduction of symptoms such as fever and cough (although not significant)
indicate that there was no increased risk of disease in the intervention group that received
chickens and produced more chickens [
27
]. This might be due to the practice of cage
utilization practiced by all households combined with enhanced awareness of the disease
risk related to chicken production and increased nutrient intake of the children through
eggs. A study in Ethiopia found no evidence of any harmful effects of the provision of
chickens on child morbidity, therefore supporting our findings [82].
To our knowledge, this is the first study to report the effect of egg intake on reducing
concurrent anemia and stunting. Much emphasis was placed on sustainability in the design
and implementation of the intervention, which is the strength of this study. The approach
of the intervention is unique and has the potential to sustain the poultry production and
egg-feeding behavior observed during the study period. However, the study had limita-
tions. The sample size did not allow us to conduct sub-group analysis, particularly among
children who were wasted and underweight at baseline, as they were too few in number
to conduct comparisons between the groups. If we had measured the children’s exposure
to chicken feces, fecal contamination of the household environment, and environmental
contamination, the study would be able to evaluate the role of cage utilization in reducing
morbidity as well as improving anemia status. As morbidity symptoms were based on
caregivers’ reports, there would be a recall bias. In addition, understanding the operational
definitions of morbidity symptoms among caregivers might be different despite the expla-
nation given, which may result in over-reporting or under-reporting of symptoms. The six
months study duration might not be enough to observe the intervention effect on reducing
morbidity symptoms.
5. Conclusions
A nutrition-sensitive child-owned poultry intervention significantly increased the
hemoglobin concentrations and reduced anemia and concurrent anemia and stunting
prevalence among under two years old children over six months of implementation. This
has a huge advantage, particularly for low-income countries that suffer from both condi-
tions well-known for their far-reaching negative consequences. In an Ethiopian context,
where iron intake is less concerning but protein and several micronutrient inadequacies
are high, whole egg consumption can play a key role in filling the gap as they provide
almost all the essential nutrients that support early life. Combined with its potential for
sustainability and model suitability for rural communities in low-income countries with
low animal-source food intake by children, the high effect sizes recorded within six months
make this approach a plausible strategy to combat anemia among infants and young chil-
dren who are the most vulnerable groups. Large-scale implementation of the model or
integration with existing interventions is warranted in rural settings where animal-source
food intake is low.
Author Contributions:
Conceptualization, A.O. and S.J.W.; methodology, A.O.; formal analysis, A.O.;
investigation, A.O.; resources, S.J.W.; data curation, A.O. and D.H.; writing—original draft prepara-
tion, A.O.; writing—review and editing, A.O., D.H. and S.J.W.; visualization, A.O.; supervision, S.J.W.
and D.H.; project administration, A.O.; funding acquisition, S.J.W. All authors have read and agreed
to the published version of the manuscript.
Funding:
This research was funded by Grand Challenges Canada (GCC), grant number R-ST-POC-
1707-05521. GCC had no role in the design of the study; in the collection, analyses, or interpretation
of data; in the writing of the manuscript.
Institutional Review Board Statement:
The study was conducted according to the guidelines of the
Declaration of Helsinki, and approved by the University of Saskatchewan’s Biomedical Research
Ethics Board and Hawassa University’s Institutional Review Board.

Int. J. Environ. Res. Public Health 2023,20, 5406 13 of 16
Informed Consent Statement:
Informed consent was obtained from all adult subjects involved in
the study.
Data Availability Statement: Data will be made available upon request.
Conflicts of Interest:
The authors declare no conflict of interest. The funders had no role in the design
of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or
in the decision to publish the results.
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