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Effect of a Child-Owned Poultry Intervention Providing Eggs on Nutrition Status and Motor Skills of Young Children in Southern Ethiopia: A Cluster Randomized and Controlled Community Trial

1. Introduction

Undernutrition among children of under five years of age is a global public health concern with the highest burden in South Asia and Sub-Saharan Africa [1]. Ethiopia, the second most populous country in Africa located at the horn, recorded rates of stunting (37%), underweight (21%) and wasting (7%) above the regional average for East Africa [2,3]. Though a declining trend was observed in the past two decades, Ethiopia is off track with progress in meeting the 2025 global nutrition targets of the World Health Assembly particularly in child stunting and wasting [1,4,5]. If the current trend continues, the country will not meet Sustainable Development Goals target 2.2. by 2030.Most of the malnutrition in Ethiopia starts after the age of six months when the children are introduced to complementary foods. Poor feeding practice is one of the important factors causing undernutrition among children under two years of age. Diets are generally cereals and lack fruits, vegetables and animal source foods (ASFs) [6]. Egg intake among Ethiopian children under two years is very low (17%) due to economic and other reasons [7]. Eggs are relatively affordable ASFs and can be made easily available through homestead poultry. Eggs are rich in various high-quality macro and micro-nutrients including protein, choline, riboflavin, vitamin B6, vitamin B12, folate, zinc and DHA as well as antioxidants and compounds beneficial for child health, nutrition, physical growth and brain development [8]. Evidence is limited on the effects of egg intake on health, nutrition, growth and development of infants and young children in low-income countries. Improved nutrient intake including protein, choline, B vitamins, lutein, zeaxanthin as well as many important minerals and overall energy intake was reported as a result of egg consumption [9,10,11,12,13]. Egg interventions have reported increased linear growth, underweight and wasting, although effects were not consistent in different settings. For instance, the results of an egg trial in Ecuador [14] could not be replicated in Malawi [15]. A reduction in underweight and anemia reported by a nutrition-poultry interventional study in Ethiopia [16] was not found in a similar community trial in Burkina Faso; rather a reduced wasting rate was recorded [17]. Only one study was found that reported the effect of egg consumption on developmental outcomes. Intake of one egg a day did not affect language, fine and gross motor milestones of young children in Malawi [18].Backyard poultry can play an important role in increasing egg intake and thereby help improve health and nutrition of infants and young children particularly in rural settings [19,20,21]. However, poultry husbandry in most rural communities of less developed countries consists of chickens living in the family house and scavenge in the surrounding environment for food [22]. Studies have associated corralling of chickens with linear growth faltering in children as a result of enteric infection called environmental enteric dysfunction (EED) that arises from repeated exposure to bacteria including Campylobacter species from the birds and their feces [23,24]. In EED, nutrients are poorly absorbed due to atrophied villi and lost due to increased intestinal permeability (leaky gut) [25]. Thus, poultry interventions that aim increased egg intake and improved health and nutrition status should consider strategies to reduce disease transmission from chickens to children [26].Our pilot trial of nutrition-poultry integrated intervention that declared chicken ownership by children and promoted use of separate chicken areas recorded a significant increase in egg intake [27] and a reduced underweight rate [16] by young children. We now report on a nutrition-sensitive poultry intervention following that approach of having a chicken gift ceremony model but includes provision of caging materials to minimize direct contact of children with the birds and their excreta. The first objective of our study was to evaluate the effect of child-owned poultry-nutrition intervention on egg intake and poultry husbandry practices, which we have recently published [28]. Therein we reported that mean egg intake significantly increased in the treatment arm (from 0.23 to 4.85 eggs/child/week) while only slightly changed in the control arm (from 0.29 to 0.40 eggs/child/week) at end line [28]. We also had the objective to assess whether promotion of egg consumption and proper poultry husbandry through child-owned poultry-nutrition intervention would positively affect growth and developmental outcomes. This paper presents anthropometry and gross motor milestone outcomes of our child-owned poultry-nutrition intervention to address this second objective.

4. Discussion

A nutrition-sensitive poultry intervention in which 6–18 months old children were owners of chickens was conducted through an innovative community-based approach. The intervention resulted in increased chicken production and improved poultry husbandry practices including cage utilization and vaccination. It also progressively and sustainably increased egg intake from 0.23 to 4.85 eggs/week/child, dietary diversity score from 2.34 to 3.34 and the proportion of children who met the minimum dietary diversity from 4.7% to 37% at end line [28]. This paper focused on the effects of the intervention on the nutritional status and gross motor development of the children. Baseline stunting, underweight and wasting rates were comparable with that of the Ethiopian mini demographic and health survey report among 6–23 months children [2]. After six months of intervention, adjusted GEE analysis showed the children’s WAZ and WHZ increased by 0.38 (95% CI: 0.13–0.63) and 0.43 (95% CI: 0.21–0.64), respectively compared to the control. In addition, the odds of underweight and stunting decreased by 54% (OR: 0.46; 95% CI: 0.26–0.84) and 42% (OR: 0.58; 95% CI: 0.37–0.91), respectively compared to control. These findings are much higher than what we reported in our pilot study [16]. A similar effect on WAZ and WHZ was recorded by a 3-arm controlled trial of nutrition-poultry intervention in Burkina Faso that stressed children’s ownership of chickens. The full intervention arm received nutrition-poultry education and chickens while the partial one received only the behavior change package. Egg intake increased from 0.1 to 6.3 eggs per week accompanied by an increase in WAZ and WHZ by 0.47 and 0.58, respectively among children in the full intervention group. The partial arm had an increase in egg intake from 0 to 2.4 eggs per week that resulted in a lesser positive effect on nutritional status which was not significant [17]. The increase in WAZ and WHZ recorded in this trial was four and five times, respectively bigger than what was found through supplementation of eggs to 6–12 months old children in rural Bangladesh [35]. One-egg-a-day supplementation in Ecuador increased WAZ, WHZ, and LAZ by 0.61, 0.33 and 0.63, respectively and reduced stunting and underweight by 47% and 74%, respectively; the biggest effect sizes reported so far from egg interventions [14]. However, these results were not replicated in the Malawi egg trial, a successor of the Ecuador study with a similar design, probably due to high fish intake in the study area [15].Despite the increase in mean LAZ score compared to the baseline and control group, stunting increased at the end line. However, our intervention demonstrated a protective effect against stunting. The increasing pace of stunting was substantially slowed and the odds of being stunted were significantly reduced. The protective effect of egg intake against stunting was also reported in our pilot study [16] and the Burkina Faso trial as stunting increased less in the full intervention arm than in the partial and control groups [17]. The intervention effect on stunting was also supported by a nutrition-sensitive agriculture study conducted recently in Ethiopia that attributed the increased LAZ score and reduced stunting to sustainable access to egg consumption [36]. The longitudinal analysis did not find significance in LAZ. However, this did not mean the intervention did not affect linear growth. Trend analysis revealed that LAZ respond to our intervention in the last two months of the study. It increased first in the fifth month and continued to the end line with a significantly higher score than the control. Several factors might have attributed to this result including the dose of egg consumption and study duration. Children in the intervention had relatively higher egg consumption during the last three months of the study period [28]; yet did not reach the level of one egg a day which was the dose used in the Ecuador trial that recorded greater results [14]. The six months study duration combined with such a trend and dose of egg intake might not be sufficient to see the effect on linear growth as was seen in a study in rural Zambia [37]. Had the intervention been implemented for longer, a greater effect of child-owned nutrition-sensitive poultry on linear growth and stunting reduction might have been demonstrated.Apart from anthropometric indicators, this study recorded a remarkable effect on the gross motor development of intervention children. Notably, running, kicking, and throwing ball milestones were attained significantly at an early age compared to control. Low nutritional status and anemia are associated with delayed motor development [38,39,40]. Both groups were delayed in attaining hands and feet crawling, walking with assistance, standing alone and walking alone milestones compared to the WHO Multicenter Growth Reference Study [30] and a longitudinal study in India on the development of children in Kashmir in the first 2 years of life [41]. The intervention effect was magnificent in attaining motor milestones, particularly running, kicking a ball and throwing a ball compared to the control. The children attained these skills at lower mean ages (17.53 ± 1.70, 18.96 ± 1.73 and 20.90 ± 1.31) in their respective order) compared to the India study (17.87 ± 2.03, 19.63 ± 3.26, 20.94 ± 3.35, respectively). Though not significant compared to the control, intervention children achieved the jump-up milestone (23.42 ± 0.7) at an earlier age than the control (23.5 ± 0.83) and Kashmir children in the Indian study (23.60 ± 1.25). Children in the control were late in attaining the running and throwing a ball and a little early in the kicking a ball and jumping up milestones compared to Kashmir children [41]. The rates of attaining motor milestones found in this study were much greater than what was recorded in the trial of water, sanitation, handwashing (WASH) and nutrition intervention in Bangladesh and Kenya [42,43].Taking the age of the children at enrollment into consideration (mean age: 10.9 and 11.4 months in intervention and control groups, respectively), the first four milestones were achieved soon after enrollment in the study by the time the children’s egg intake was low, at least not sufficient enough to have an effect on motor development, though improved from the baseline. Our intervention showed a remarkable effect on those milestones that the children achieved after they had higher egg intake for longer periods relatively supporting the evidence base that diet has a significant contribution to children’s motor development. Nutrition factors including complementary feeding frequencies, dietary diversity, and egg and oil intake were significant predictors of earlier achievement of motor and language development outcomes among young children in Haiti [42]. Rate of attaining motor and other developmental milestones increased when the nutrition component (lipid-based nutrient supplementation and IYCF counselling) was added to the water, sanitation and handwashing (WASH) intervention in Bangladesh [43]. Meat and other types of ASFs consumption in Nepal [40], dietary diversity and intake of iron-rich foods in Bangladesh [44], intake of lipid-based nutrient supplements in Ghana (LNSs) [45] and Burkina Faso [46] and home fortification with LPS and/or micronutrient powder in Bangladesh [47] were associated with better motor and other developmental milestones. On the contrary, the LNS trial in Malawi, a replica of the Burkina and Ghana studies, showed only a marginal effect [48]. Provision of one egg a day also had no effect on child development in Malawi [18]. This happened probably due to chance as explained by both studies, high fish intake as stated by the egg trial or other unknown factors.The improvement in the nutritional status of the children in this study might have contributed to their motor development as there is a positive relationship between nutritional status and gross motor skills. The significant contribution of nutritional status on gross and fine motor skills development was revealed by a study in Indonesia that nutritional status explained 41.8% of child’s gross and fine motor skills with a correlation value of 0.650 [49]. Increased weight-for-age [38,50], height/length-for-age [38,40,50,51] and weight-for-height/length [38,40] were associated with and found to be important predictors of motor and other domains of development including language skills.Eggs provide several nutrients critically essential for early growth and development. Studies reported that egg intake was associated with higher intakes of total protein, total fat, monounsaturated fat, polyunsaturated fat, cholesterol, phosphorous, Vit B12, D and E, pantothenic acid, biotin, choline, lutein and zeaxanthin, α-linolenic acid and docosahexaenoic acid [13,52]. Prevalence of inadequacy was also found to be lower among egg-eaters than non-egg-eaters for Vit A, E, D, B5, B12, riboflavin, zinc, iron, selenium and choline [52,53]. However, there are several nutrients such as vitamin c, B vitamins, calcium and iron that are not found in high quantities in eggs; thus, need to be fulfilled by other sources [52,53].Although all nutrients are important for growth and development, nutrients particularly protein; zinc; iron; choline; folate; iodine; vitamins A, D, and B12; and long-chain polyunsaturated fatty acids including docosahexaenoic acid and arachidonic acid play an indispensable role in neurocognitive development [54,55,56]. Early infancy deficiency of these nutrients is associated with long-term neurobehavioral damage that may not be reversible by nutritional therapy [57]. On the contrary, early supplementation is associated with improved neurodevelopmental outcomes over an extended period of life. Children in Guatemala supplemented with a high protein high-calorie drink at an early age recorded higher scores on tests of general knowledge, numeracy, reading, and vocabulary along with faster reaction time in information-processing tasks than those provided with no protein low-calorie drink eleven years after the intervention stopped [58]. A choline supplementation study among children with fetal alcohol spectrum disorder also found significant neurodevelopmental benefits including non-verbal intelligence, higher visual-spatial skills, higher working memory ability and better verbal memory compared to the placebo group after four years of the trial completion [59]. Eggs are excellent sources of protein, choline, Vit B12 and long-chain polyunsaturated fatty acids. Their contribution of zinc, folate and Vit D to the daily requirements of infants is also remarkable. Thus, the consumption of one egg a day at an early age of complementary feeding probably might have long-term benefits in neurodevelopment besides the reported positive short-term outcomes on growth and motor development.We deemed the improved poultry husbandry practices documented in the intervention group, particularly the cage utilization [28] magnified the effects recorded on child growth and development. In our pilot study in which we gave education on the danger of chicken feces promoting separate chicken shelters and sanitation of the household environment, we found encouraging results on child health and nutrition outcomes through increased egg intake, but effect sizes were less than what we found in this trial [16,27]. In the current study, after the provision of caging materials, keeping chickens in a shelter separated from the family house or inside a night coop placed in a corner of the family house was widely practiced. The night cage was movable, easily cleaned and small in size so that children could not climb inside, unlike the one used in the Peru study which was installed in the family house causing accumulation of chicken feces and the probable entrance of children into the coral [60]. The chickens were kept in an enclosure during the day that, together with the night coop/separate chicken shelter, might have minimized children’s contact with the chickens and their excreta. However, we did not collect information on exposure of children to chicken feces. Chickens are important reservoirs of Campylobacter bacteria that cause enteric infection in children. Studies reported an association between poultry keeping with stunting highlighting the importance of keeping chickens in separate shelters or cages [23,26]. Taking the benefits of egg intake in improving early childhood growth and development into consideration, homestead poultry is a recommended intervention particularly in rural settings to increase egg availability for consumption. When integrated with nutrition education, backyard poultry, regardless of the flock size, plays a great role in increasing egg intake sustainably among children [61]. The Ecuador trial result was no more found after two years as only a few households continued the practice of egg feeding because the intervention was based on egg supplementation [62]. Our intervention gave due emphasis to the sustainability of child-owned chicken production and egg-feeding practice which is the strength of this study. Existing government structure and personnel from the district to community level were utilized; religious and community leaders were engaged from the beginning, and efforts were made to build the capacity of frontline implementers and families in egg feeding and baby-friendly poultry. The unique approach through which the children were enabled to own chickens is also the strength of our trial that, we believe, helps sustain poultry production and egg-feeding behavior. The study duration might have limited our trial to see the intervention effect on LAZ. The wide age range of target children and the sample size was not ideal to assess the intervention effect on motor development, particularly hands and feet crawling, walking with assistance, standing alone and walking alone milestones. A further limitation was that gross motor milestones were collected by HDTLs, not experts in the field. We provided them with two days of practical training before they were first deployed for data collection and a skill-reinforcing training monthly. However, taking the nature of milestone assessment into account, the successive training we provided them with might not be good enough to gather quality data. Finally, we lacked information on children’s exposure to chicken feces and thus we could not ascertain the role of cage utilization in improving child health and nutrition.

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