Soil-transmitted helminthiases (STHs) and schistosomiasis are among the most common parasitic infections worldwide. They affect more than one billion of the world’s poorest people 1. Globally in 2010, 819 million roundworm (Ascarislumbricoides), 464.6 million whipworm (Trichuris trichiura), and 438.9 hookworm (Necator americanus, Ancylostoma duodenale) were reported in Asia (70%), Sub-Saharan Africa (16%) and other part of the world 2. Globally, there are around 200 million Schistosoma infected people with 160 million living in Sub-Seharan Africa (SSA) 3. According to recent estimates, over 267 million pre-school age and 568 million school-age STH infected children are found in the world with more than 1.5 billion people infected by these infections 4. According to food and agriculture (FAO) estimates, around 1.02 billion people are undernourished worldwide 5. In spite of the efforts targeted at reducing malnutrition and hunger by Millennium Development Goals, there has not been any significant improvement 67. About 50% of all deaths among global children is related to malnutrition 8. Malnutrition related with intestinal nematodes and other parasites was reported as a major factor in reducing physical, cognitive, and educational development in children while causing decreased fitness, cognition and work productivities in adults, outside the mortalities related to this complication 91011. The mechanisms by which these intestinal helminth infections aggravate malnutrition (protein energy malnutrition, anaemia and other nutrient deficiencies) include anorexia (loss of appetite), malabsorption and decreased food intake due to nutrient loss through bleeding, vomiting or diarrhea 111213. Decreased barriers protection and impaired immune function during malnutrition can, in turn, aggravate the incidence of intestinal parasite infections 13.

In Ethiopia, intestinal parasitic infections have been reported as the cause of malnutrition, anemia and growth retardation among children under 5 years of age 1415. Factors that increase the risk of intestinal parasitic infections such as swimming, bar foot walking (lack of shoes), bad hand washing habits and low education status of parents were also reports to be associated with malnutrition 161718. Researches describing the role of helminth infections and their intensity on malnutrition, anemia and normal haematological indices in primary school children are rare. The aims of this research was to evaluate the impact of intestinal helminthes (infections and intensities) on the malnutrition, anaemia and haematological indices of school children in Azezo primary school in Gondar town.

Following ethical approval by research ethical review board of University of Gondar and permission letter obtained from Azezo – Teda sub-city administration to conduct this research in Azezo government elementary school, study participants were recruited for the study. This elementary school was selected purposefully as it has students coming from both urban and rural areas and high prevalence rate of helminth infections. A stratified random sampling method was used to select the study participants based on their grade level. A rotary method was used to select the total number sample required for the study from all students attending from grade 1 up to grade 8. The students were participated in the study after the purpose and a benefit of the research explained to their parents or guardians and written consent was obtained. Only students willing to participate in the research were included. The students could also withdraw from the study at any time during the execution of the sampling process

Data about socio-demography and the possible risk factors were collected using questionnaire before the results for malnutritional indices, intestinal helminth infection and haematological tests obtained. The datab collected was cleaned in an Excel spread sheet before transferred to statistical package for social sciences (SPSS) version 20 for statistical analysis. Descriptive statistics was used to analyze the prevalence of the different outcome variables. Mann whitnay test (non-parametric analysis of variance (ANOVA)) was used to determine the existence of gender or age group related statistically significant difference for intestinal helminth infection, intensity of infection, co-infections, infecting species, anaemia, stunting, wasting and haematological categories in the school children. Binary logistic regression test was used to see association between intestinal helminth infection, anemia, stunting,, wasting, age groups, malnutrition indices and haematological categories. Multiple logistic regression analysis was used to determine the likelihood of anemia or odd ratio (OR) in school children, when it was compared with uninfected, mono-infected, coinfected and species of intestinal helminth. For the statistical analysis, p-value < 0.05 was considered as significant different for 95% confidence interval.

A total of 384 school children (179 (46.7%) males and 205 (53.3%)) females) were recruited in this study with age ranged from 7 to 15 years. Of the total school children, 39.3% (151) were in 7-10 years age group while 60.7 % (233) were in 11-15 year age group (Table 1). Mean ± St.D (Median) (range) for height and weight for the all ages were 140.93 cm ±11.4 (140) (114-178) and 30.6 kg ± 7.3 (29.50) (15-55) respectively. Linear increase in height and weight for different age from age 7 to 15 were observed in statistically significant different manner for mean (P=0.000) and median (P=0.000) values.

The overall prevalence of helminthes infections in the school children was 45.8% (178/384) with 56 light, 47 moderate and 75 heavy infections (Table 2). Ascaris infection (20.6% or 79/384) was the leading infection. The second and third leading infections were Schistosoma mansoni and hookworm infections with prevalence of 17.4% (67/384) and 13.3% (51/384) respectively. The prevalent of the remaining Tricuristrichura, Hymenolopis nana and Taenia spp were 3.4%, 1% and 0.3% respectively. Of the total 178 school children found infected, 37(9.6%) were with double infections (15 Ascaris – Schistosoma, 12 Ascaris – Hookworm, 4 Schistosoma – Hookworm and 6 Ascaris and others) and 5 (2.8%) were with triple infections (4 Ascaris –Schistosoma – others and 1 Ascaris - Hook worm –Tricuristrichura).

Of the total school children analyzed for body mass index for age Z scores (BAZ), 37(9.6%) were very sever thin (sever wasted) (Z scores < -3SD), 66 (17.2%) sever thin (wasted) (-3 SD < Z < -2SD), 147 (38.3%) thin (-2 SD < Z < -1SD), 132 (34.4%) normal (−1SD < Z 2SD). Only 34. 4% were included with in the 25th and 75th percentiles of the WHO normal distribution curve. Of all heights for age analyzed, 7(1.8%) were severely stunted (< - 3 SD), 40 (10.4%), stunted (< -2SD), 334 (87 %), normal height for age (-2SD > Z < 2SD) and 3(0.8%) more height for age (> 2SD). Only 87 % were included in the 15th and 85th normal curve range. Gender showed no statistically significant differences (p>0.05) for BAZ and HAZ scores (table 3). The prevalence of overall stunting in 7-10 age group was 0.7% (1/146) compared to 19.5% (46/236) in 11-15 age group. Stunning was statistically significantly different in 7-10 and 11-15 age group intervals (p=0.000). Of the total 47 school children with stunted growth, 25(53%) were male while the 22 (47%) were female. Statistically significant difference was not observed (p=0.7) for gender. Of total 47 stunted school children, the percentage with light, moderate, heavy and none infections were 34%, 4.3% 12.8% and 48.9% respectively. Of 337 school children who were not stunted, and the percentage with light, moderate, heavy and none infections were 11.9%, 13.4%, 20.5% and 54.3% respectively.

Ascaris lumbericoides, Schistosoma mansoni and Hookworm mono-infection or Ascarislubericoides – Schistosoma mansoni and Ascaris lumbericoides – Hookworm co-infections were statistically significantly associated (P≤0.001) with protein malnutrition (hypoproteinemia) and anaemia compared to non-infected school children. The overall infection was also statistically significantly associated with hypogycocemia, hypoproteinaemia and anemia (p=0.000) (Table 4). Intestinal helminth infections, intensity, mono or coinfections between stunted and normal school children were not statistically significantly different (P>0.05). Mann – Whitney analysis of variance indicated intestinal helminth infections were not statistically significantly different (p>0.05) for different gender. Intestinal helminth infections were highly prevalent in rural (57.1%) compared to urban residence (30.1%) in statistically significant different (p=0.000) manner. Swimming or washing in the rivers were also more common for rural residences (p=0.04). But, Swimming or washing in the rivers were not associated with stunting, wasting and anaemia (p>0.05). The prevalence of anemia in females was 32.6% compared to 29.1% in males. Anemia was not statistically significantly different for gender (p=0.17). The prevalence of hypo-glycemia and hypo-proteinaemia were high in anemic school children compared to normal in statistically significantly different manner (p<0.05). The prevalence of anemia in intestinal helminthes infected school children was 60% compared to 8.3% in non-infected children and the difference was statistically significant (p=0.000). The incidence of anemia was 12 times higher in intestinal helminthes infected school children compared to non-infected. In school children with below normal MCH values, 61.3 % were anaemic compared to only 25.6% in school children with normal MCH values (27 – 30 pg). In school children with below normal MCHC values, 44.8% were anaemic compared with only 25% in school children with normal MCHC values (33 -38.5 g/dL). Statistically significant differences were observed in prevalence of anemia between school children with below normal and normal MCH and MCHC vales (P≤0.01) (Table 5).

Discussion

In school children, chronic schistosomiasis contributes to anemia and under-nutrition, which, in turn, can lead to growth stunting, poor school performance, poor work productivity, and continued poverty while blood loss due to hook worm infection can cause iron deficiency anemia and hypo-proteinaemia 26. Heavy S. mansoni infected children in Brazil (above 400 eggs/g of stool) showed 2.74 fold higher risk of stunting compared to uninfected children 27. Ascariasis cause malnutrition in addition to pathology associated the worm migration in the body. Chronic dysentery associated with trichuriasis is also a major problem in malnutrition and health of school children 28. Ethiopia, the second populous nation in Africa, has been classified as low income countries with 20% of people living under poverty in both urban and rural areas 29. Low socioeconomic status or low accessibility of food (poverty) in Ethiopia could be the main cause of malnutrition 3031 similar to this study result. Factors that increase the risk of intestinal parasitic infections in Ethiopia such as swimming, bar foot walking (lack of shoes), bad hand washing habits and low education status of parents were also reports to be associated with malnutrition 18. In Ethiopia, intestinal parasitic infections in children are reported to be associated with malnutrition, anaemia, and growth retardation 32.

The prevalence of stunting related to malnutrition in under 5 years in Ethiopia reduced from 64% in 1990 to 47% in 2008 before further reduction to 40.4% in 2014 333435. The prevalence of intestinal helminthes infections in this study (45.8%) is lower than the previous report (2008) in another Azezo primary school (72.9%) 18. The reduction in the intestinal helminth infecions could be due to the recent regular deworming program in the primary schools.

Ascaris lumbericoides, Schistosoma mansoni and hookworm mono-infection in addition to Ascaris lubericoides – Schistosoma mansoni, Ascaris lumbericoides– Hookworm co-infections and triple infections were statistically significantly associated with protein malnutrition (hypo-proteinemia) and anaemia compared with none infected school children (P ≤ 0.001). This type of association in which intestinal helminthes infections aggravate the situation of malnutrition was reported to be common in children 36. Prevalence of stunting and anaemia were reported higher in male than in female in Kenya 37. But, gender did not show any difference (p>0.05) for prevalence of stunting or anaemia in the school children studied (Table 4). The prevalence of anaemia was affected by the species and intensity of infections of intestinal helminthes in statistically significant ways (p=0.000) compared with none infected school children. The likelihood of anemia in school children, when it was compared with uninfected, increased 148 times for both Ascaris lumbericoides-Schistosoma mansoni co-infection, 38 times for Hook worm, 20 times for Schistosoma mansoni and 3 times for Ascaris lumbericoides mono-infection. But in Kenya S. mansoni mono-infection was reported to associate with anaemia and the likelihood of anemia in Schistosoma infection was 3.68 times compared with non- infected children 37.

Except for one school child (0.3%), there was no problem of overweight in the current study in school age children. Only 34.9% of the school children were with in WHO normal range based on BAZ scores. Majority (65%) were in state of thinness or underweight (thin, wasted or sever wasted). Thinness (underweight) were not statistically significantly associated (p>0.05) with age and sex. All these results could show malnutrition was very common in all children and might be related with the low socio-economic background of the community in Azezo areas and high prevalence of intestinal helminth infections. Poverty related malnutrition, most probably, have additional effect on intestinal helminth and Schistosomamansoni infections development of school age children in Ethiopia as opposed to previous report which stated the widespreaded prevalence of intestinal parasitosis and malnutrition among school children in Ethiopia were not associated with anaemia and/or stunting 38. According the study conducted in school age children in Fincha’a sugar estate in western Ethiopia where children regularly dewormed and get relatively good health facilities, poverty (lack of job) was the source of stunting compared to Schistosoma mansoni infection which is the most important problem in the areas 39. The lack of any effect of intestinal helminth and Schistosomamansoni infections pus malnutrition on stunting and/or underweight in Zegie Peninsula villages (northwestern Ethiopia) located on or near Lake Tana 40, most probably, related to the effective regular deworming process and easy access to get fish to use as food.

In this study, analysis of HAZ scores showed 97.9% of the stunting in the school age children was found in 10 - 15 years age group compared to 2.1% in 7-10 years age group (p=0.000). Similar statistically significantly different (p=0.000) for high stunting prevalence (56.4%) in 10-15 age group compared to lower (33.6%) in 5-10 age group was reported in school children in Macha district in Northwest Ethiopia 41. A total of 50.1% stunting in 12-14 age group school children compared to 36.9% in 6-11 age group (p=0.000) was also reported in Arbaminch town (Southern Ethiopia) 42. Frequent stunting in children above 10 years compared to those under 10 was reported in Angola due to prolonged problem of food shortage during previous war time 40. From the fact that anemia prevalence, glucose or protein malnutrition were not different between the age groups (p>0.05) (almost the same probability) in addition to lack of difference in incidence of intestinal helminth infections between stunted and normal school children (P=0.49), most probably, stunting was the result of prolonged malnutrition related to poverty and parasitic infection and re-infection during early childhood. Stunting may not be restricted to areas with war and prolonged shortage of food as indicated by Olivera et al 43. Prolonged malnutrition and infection and re-infection of intestinal helminth in developing nation could be the main source of stunting.

Probably, swimming habits of school children in the rivers in the study areas, unhygienic and bare foot walking habits mentioned during previous study 18 could be the important risk factor for high prevalence of intestinal helminth infections and anemia in Azezo school children. High incidence of Ascaris lumbercoides, Schistosoma mansoni and hookworm infections were statistically significantly associated with lower MCH values (P≤0.001). Similarly, Schistosoma mansoniand hookworm infections were associated with below normal MCHC level (p=.000). Below normal concentration of MCH and MCHC were statistically significantly associated with anaemia (Table 5). Similar study in Thailand has indicated statistically significantly lower (P<0.000) MCH, and MCHC levels in helminthes infected group compared to the helminth-free group 4044.

Helminth infection is associated with anaemia and hypo-proteinaemia, lower MCH and MCHC levels. The likelihood of anemia is very high in mono-and co-infected compared to uninfected school children. Stunting is the product of prolonged malnutrition and repeated reinfection of intestinal helminth infections in school children. Intestinal helminth infections most probably aggravate the malnutrition in school children with low accessibility of food supply. Regular monitoring of nutritional status of school children and screening and treating intestinal helminthes are required including school feeding, deworming, clean water supply and public health awareness.

Normal ranges of haematological and biochemical values obtained from literatures were used as reference to classify the results of this study due to lack of normal range values specific for school –age children in Ethiopia.

University of Gondar, office of research and community service,has funded this research.

MB, DT and LW designed the research and participated in the research. DT collected the samples and processed them. MB and WL supervised the processes. DT and WL analuzed the data. WL prepared this manuscript.