Intestinal helminth infections and dietary diversity score predict nutritional status of urban schoolchildren from southern Ethiopia

In developing countries, childhood undernutrition is a major public health problem with schoolchildren and adolescents among the most vulnerable groups [1]. Worldwide, 159 million children are estimated to be stunted and 50 million suffer from acute malnutrition with the majority living in the developing world [2]. Even though stunting mostly occurs during the first 2 years of life [3], it continues to accumulate throughout the school years [4]; whereas acute malnutrition and micronutrient deficiencies are among the most recurrent health problems in schoolchildren [5]. The adverse effects of malnutrition in schoolchildren are not limited to poor health and physical growth, but also hamper intellectual capacity, social skills and school performance with far reaching consequences on future economic and human development of societies [6–11].

Multiple and complex factors contribute to malnutrition and poor growth of schoolchildren with poor nutrition and infections being the immediate causes [12]. Studies showed dietary factors like low meal frequency [13], consumption of less diverse diet [14], inadequate intake of carbohydrates [15] and household food insecurity [15] are important determinants of nutritional status in schoolchildren. Recurrent childhood illnesses like diarrhea, respiratory infections and intestinal parasites also contribute to malnutrition through decreased food intake, impaired nutrient absorption, direct losses and stimulation of the immune system that diverts energy and nutrients from structural and physiological functions [16, 17]. The impact of intestinal parasite infection on nutritional status of schoolchildren has received special attention considering its high prevalence and recurrent occurrence in this age group [18]. Studies found higher stunting and underweight risk among schoolchildren with hookworm infection, trichuriasis and ascariasis [15]. Family wealth, maternal education, household size, and age and sex of a child are among the several socio-demographic predictors of malnutrition commonly reported in studies from developing countries [13, 15, 19].

In Ethiopia, the most recent nationwide survey reported that significant proportion of schoolchildren and adolescents are malnourished with stunting and wasting prevalence of 23 and 22%, respectively [20]. On the other hand, limited nutrition policy and program attention has been given to this age group partly due to the lower magnitude and mortality risks compared to preschool children. However, the period of school age and adolescence is the time where nutritional insults continue to result in long term consequences and is the last opportunity to compensate early growth faltering and associated consequences [21–24]. The limited attention given to the problem includes the lack of available evidence on the nutritional status and the important modifiable risk factors among schoolchildren living in different social and environmental conditions in the country including in the current study area. Therefore, we aimed at determining the magnitude and predictors of undernutrition among schoolchildren in Arba Minch town, southern Ethiopia.

Of the 532 schoolchildren sampled, data was collected from 511 (96.1%) whereas the remaining 17 children were not found during data collection and 4 were older than 14 years. Mean (SD) age of the study participants was 10.6 (2.4) years with majority (63.6%) between 10 and 14 years. Most (86.3%) of the children were living with both of their parents, whereas 70 were living with one of their parents (10.5%) or with other people (3.1%) like grandparents, relatives or fosters. Majority of participants’ households were male headed (87.9%) and with family size of at least 5 people (64.8%). About two-third (65.8%) of the study children were from food insecure households and more than half (55.0%) of them had a DDS of ≤ 4. During the 2 weeks prior to the study, 169 (33.1%) of the participants experienced illness including diarrhea (40.8%), acute febrile illnesses (38.5%) and acute respiratory infections of which only 81 (47.9%) received medical care. Intestinal parasite infection was detected in 285 (55.8%) children of which 87 (17.0%) had more than one infection. Regarding the type of parasite infection found in children were, A. lumbricoides 107 (37.8%), Hookworms 75 (26.6%), T. trichiura 54 (19.1%), H.nana 44 (15.6%), G.lamblia 42 (14.8%), Taenia spp. 24 (8.5%), E.histolytica 23 (8.2%), S.mansoni 11 (3.9%), E.vermicularis 9 (3.2%) and S.stercoralis 2 (0.7%).

The mean (SD) HAZ and BAZ of the study participants were -1.37 (0.94) and -0.63 (1.06), respectively. The prevalence of stunting (HAZ < -2SD) and wasting (BAZ < -2SD) were 26.0% (95% CI: 22.3, 30.1%) and 11.7% (95% CI: 9.1, 14.9%), respectively. The prevalence of severe stunting (HAZ < -3SD) was 3.7% (95% CI: 2.3, 5.7%) and severe wasting (BAZ < -3SD) was 2.9% (95% CI: 1.7, 4.8%).

The current study found stunting and wasting prevalence of 26 and 12% among schoolchildren in Arba Minch town. The magnitude of stunting in this study was comparable with the nationwide estimate (22%) for the same age group and reported in other studies in Ethiopia [15, 20, 33]. On the other hand, acute malnutrition as indicated by wasting was relatively low compared to the nationwide prevalence (23%) and other studies which could be due to a lesser drought and related nutritional insults in the study area compared to some areas of the country [20, 34]. Stunting was higher among boys than girls (30 vs. 22%; p-value = 0.037); a similar finding to previous studies from Ethiopia and other countries [1, 13, 20]. This could be due to earlier start of adolescent growth spurt in girls that may compensate to some extent for prior nutritional insults. A study on African schoolchildren showed stunting persists in boys until the age 16 years whereas for girls compensatory growth occurs starting from 12 years [35]. Poor household wealth, lack of maternal formal education, large family size (≥5), low DDS (≤4) and intestinal helminth infections were found to be the important predictors of chronic malnutrition (stunting) among the schoolchildren, whereas poor household wealth, not living with both parents and recent illnesses independently predicted acute nutritional status (wasting).

Intestinal helminth infections were the most important independent predictors of stunting status among the variables assessed in this study. The odds of stunting was 5 times higher among the schoolchildren infected with A.lumbricoides [AOR (95% CI) = 5.0 (2.7, 9.4)], 8 times higher in the presence of hookworm infection [AOR (95% CI) = 8.0 (4.0, 15.8)] and about 6 times more in children with T.trichuria infection [AOR (95% CI) = 6.3 (2.8, 14.1)]. This finding is consistent with what has been reported in previous surveys [15, 36] and intervention studies that showed improved growth performance after schoolchildren were treated with anthelminthic drugs [37–40]. Intestinal helminth infections could affect linear growth and nutritional status through several mechanisms including decline in food intake [39, 41]; nutrient wastage from blood loss, malabsorption and diarrheal episodes [41, 42]; and suppression of hormones required for bone growth like the growth hormone (GH) and insulin-like growth factor-1 (IGF-1) [43]. The WHO recommends regular school-based deworming programs with a target to cover at least 75% of school-aged children at risk by the year 2020 [44].

Low child DDS (≤4) in the current study was significantly associated with stunting status [AOR (95% CI) = 2.3 (1.2, 4.7)] suggesting that a diet habitually low in micronutrients may have contributed to stunting in the current study. DDS is a recommended qualitative indicator of micronutrient adequacy of a diet [27, 45] and has been shown to predict growth of children in other studies [14, 46, 47]. On the other hand, DDS was not independently associated with wasting status; a similar finding to previous studies that reported DDS was associated with stunting, but not with wasting [14, 46, 47]. DDS may not necessarily reflect variation in energy intake of children as a child may have optimal energy intake from a monotonous starch based diet with low diversity. Other factors resulting in acute nutritional insult like recent illnesses might also attenuated a possible association between diet and wasting status in our population.

Children from food-insecure households had significantly higher stunting and wasting than their counterparts from food-secure households, but the association disappeared while adjusted for important covariates in the multivariable models. We also found weak association between household food-security status and dietary quality of our children; of children with low dietary quality (DDS ≤ 4), 49.1% were from food-secure and 58.0% were from food-insecure households. These findings suggest that dietary inadequacy among schoolchildren in this study transcended beyond household food security status. Additional factors like poor quality of available foods, lack of awareness about balanced diet and intra-household food maldistribution could have affected efficient utilization of available household resources that highlights the importance of nutrition education about the importance of diverse and nutritious diet to support optimal health and growth of schoolchildren.

Among the socio-demographic factors, lack of maternal formal education, large family size (≥ 5), poor household wealth and not living with both parents were important predictors of undernutrition in our study population, as was the case in studies reported elsewhere [13, 15, 19, 34, 48, 49]. Education of mother’s on health and nutrition has been shown to play an essential role in the practice of diversified food consumption, health care seeking behavior and utilization and generation of income [50]. It is also reasonable to assume that stunting is more prevalent in children from large families since resources including food, nurturing and health care could be constrained [13, 15, 48]. Living with a single parent could also affect access to resources and time available for child care.

Stunting reflects a chronic nutritional insult that majority occurs during the early years of life. On the other hand, in the absence of direct health and nutrition interventions, early growth faltering tends to persist and further accumulates throughout the school age and early adolescence [4, 21, 51]. This time of the lifecycle also opens the opportunity to curb lost growth during early life and break the intergenerational cycle of malnutrition. The pubertal growth spurt is the period of the second most rapid growth providing the last chance to intervene before final height is attained [52]. Longitudinal follow-up of children in developing countries showed stunted children could catch-up with their genetic potential at least partially between 8 and 15 years suggesting investment during this time may have a potential return both at individual and societal levels [21–24]. However, this opportunity could be missed by poor health and dietary factors that can cause further nutritional insult and limit the potential for catch-up growth. The current study showed high prevalence of undernutrition among schoolchildren where direct health and nutrition program targeted to schoolchildren is not available. Effective public health and nutrition interventions are required to alleviate nutrition and health problems of the schoolchildren and associated adverse effects on health and schooling. A comprehensive school-based health and nutrition intervention including prevention of intestinal helminth infections through regular mass deworming activities and promoting personal hygiene and balanced diet in skill-based health and nutrition education involving parents may help to address the problem in the current study population.

In this study, we used a school-based sampling of study participants though the high primary school enrollment rate in the study area improves generalizability of our findings to all children in the community. Dietary Diversity Score of children was based on caretakers’ recall of the previous day intake which did not include foods consumed outside home. However, food consumption outside home was not common among the target age group in this community. We also did not control for past nutritional status of children in our analyses.

The current study showed that both acute and chronic malnutrition are prevalent among schoolchildren in the study area. High prevalence of intestinal parasite infections, poor dietary quality and common illnesses are the important modifiable risk factors for undernutrition among schoolchildren in the current study.