1. Introduction

The term parasite is defined as an organism that finds its ecological niche in another organism, and they are the causes of morbidity and mortality throughout the world, particularly in developing countries. According to Sitotaw and Shiferaw [1], the most common intestinal protozoan parasites in children are Entamoeba histolytica, Giardia lamblia, and Cryptosporidium species. In addition, there are intestinal helminth parasites that are known as geo-helminths and soil-transmitted helminths, namely, Ascaris lumbricoides, Trichuris trichiura, Ancylostoma duodenale, and Necator americanus. As stated by the WHO, about 24% (1.5 billion) of the world’s people have been infected with intestinal parasitic infection, mainly hookworms, Ascaris lumbricoides, and Trichuris trichiura, and the prevalence of intestinal parasitic infection surpasses 50% in several areas of sub-Saharan Africa [2]. In Ethiopia, the overall status of parasitic infection was 46.88% in children with diarrheal disease. The most prevalent protozoa, Giardia lamblia (9.38%) and Entamoeba histolytica/dispar (6.25%), were observed with the highest infection rates in the age groups that varied from 6 to 10 years old [3]. Infections with IPs are not only responsible for morbidity and mortality, but they also cause nutritional problems (such as stunted growth, low vitamin A, iron deficiency anemia, weight loss, and chronic blood loss) and compromise psychological and social well-being. In addition, Feleke et al. [4] described that mental developmental impairment is also another public health challenge of IPIs, particularly in children (such as impaired growth, decreased school attendance, cognitive impairment, decreased educational achievement, and adult productivity).

According to the WHO report, the term malnutrition generally refers to both undernutrition and overnutrition, and anthropometric indicators (AI) that are commonly used to measure undernutrition in a population are stunting, wasting, and underweight [5]. Worldwide, the prevalence of undernutrition is great, and its consequence in terms of public health is alarming. In 2016, as WHO reported, it is estimated that 178 million children are undernourished, 20 million children are suffering from the most severe form of undernutrition, and 3.5–5 million annual deaths are occurring among children aged 6–59 months [6]. One form of malnutrition that is currently a global problem is stunting. Stunting is an impact that occurs due to chronic malnutrition and is a major problem for children in rural areas who experience developmental disabilities [7]. It has also resulted in the loss of adult height by 3%. Subsequently, childhood stunting might end up with a 1.4% loss in productivity [8]. Several studies have been conducted in Ethiopia to assess the prevalence of IPIs in children but failed to associate them with undernutrition [1, 9, 10]. Moreover, studies have found relationships between intestinal parasites and malnutrition in children [11, 12]. There is also limited evidence of the magnitude of undernutrition among children in the Bele Gesgar area. Therefore, this study was carried out to identify the recent burden of intestinal parasitic infection and its associated risk factors among malnourished children in Bele Gesgar Primary Hospital.

2. Materials and Methods

3. Data Analysis

In this study, the data was analyzed using SPSS software version 26. The obtained values were considered significant at p < 0.05 in all the analyses. In addition, univariate and multivariate logistic regression analyses were considered to identify significant risk factors for parasitic infection among the study participants. The comparison among the proportions was also analyzed using the chi-square test (MedCalc Software Ltd., Comparison of Proportions Calculator).

4. Quality Control

In order to be certain of the quality of the obtained data, all the positive specimens were re-examined, and 10% of the negative specimens were randomly selected and re-examined by experienced laboratory technicians who did not have any information about the previous results. In addition, for quality checkup purpose, the control slides were also used during each run of the stain examination.

5. Results

6. Discussion

Intestinal parasitic infections and undernutrition have continued to be major public health problems in Ethiopia, especially among children of various age groups. Thus, assessing IPIs and nutritional status of children is essential for improving the health conditions and academic performance through implementing appropriate intervention strategies [20]. Therefore, the present study was conducted to assess the magnitude of IPIs in malnourished children, compare them with those of nonmalnourished children, and determine the associated risk factors among children. In this study, 11 parasites were detected, namely, Entamoeba histolytica/dispar, Giardia lamblia, Ascaris lumbricoides, hookworm (Ancylostoma spp.), Taenia spp., S. mansoni, Trichuris trichiura, Enterobius vermicularis, Hymenolepis nana, Cryptosporidium spp., and Cystoisospora belli. Among the detected parasites, Entamoeba histolytica/dispar was the major parasite observed in malnourished children, showing a significant difference with nonmalnourished children (p < 0.05). The current study showed no difference between the two study groups except for the Entamoeba histolytica/dispar, which showed a significant difference (p < 0.05), showing that it is the most prevalent protozoa. This is in line with the study conducted by Bisetegn et al. [11] and a study conducted in Iraq that reported E. histolytica as the most common child-infecting protozoa, followed by G. lamblia, H. nana, and E. vermicularis [21]. The highest prevalence of E. histolytica/dispar may indicate the fecal contamination of foods and drinks and poor hygienic practice in the community. On the other hand, the predominance of E. histolytica/dispar infection might be associated with poor hygiene, poverty, lack of access to portable water, and a hot, humid tropical climate. Furthermore, their infective stage (the cyst) can withstand a standard level of chlorine treatment in drinking water [22].

The total parasite infection was higher in malnourished children as compared to well-nourished children, showing a statistically significant difference (p < 0.05). This indicated that the parasitic infection is more prevalent in undernourished children, and the nutritional status of a child is the best indicator of the child’s overall health conditions [23]. IPIs harm the nutritional status of the infected individuals, and they may trigger bleeding of the gastrointestinal tract and nutrient competition, which may also lead to nutrient malabsorption [24]. Children with malnutrition and compromised immune systems are more susceptible to parasitic infections, which further weaken the immune function, perpetuate the cycle of infection, and increase malnutrition [25].

In addition, the overall prevalence of IPIs was variable among the studies conducted by different researchers in different countries. For example, our recent result of IPIs in undernourished children (44.07%) is lower than the study conducted by Onyemelukwe et al. [24], which was 51.8%, and it is higher than previous studies in Guinea (27%) among the malnourished children [26] but lower than 58.3% in Oscoda Lagos [23], 67.4% in Akwa Ibom Nigeria [27], and 52.4% in Ethiopia [20]. This difference might be due to environmental and geographical variation, differences in the study seasons, sanitation, hygienic practice, implementation of deworming, and poor supervision of children. Moreover, taking repeated stool samples could increase the chance of recovering multiple intestinal parasites.

This study also showed the existence of double infection and triple infection of parasites between the two studied groups (i.e., malnourished and well-nourished children). The study indicated that the prevalence of coinfection was higher in malnourished children as compared to the well-nourished children. This might be associated with different factors that may exist between the study participants. Environmental conditions could have an impact on host physiology and susceptibility to intestinal parasitic infections. For example, a stressed or malnourished host is more likely to be infected. In addition, host life history traits such as growth rate, lifespan, and fecundity have also been shown to favor coinfection in humans [28]. Interestingly, we found a low status of coinfection as compared to the study conducted by Zhang et al. [29] in southwest China. This might be due to the variations of the study area and methods employed in the detection of the parasites and the level of expertise in parasite identification. In addition, coinfections could either have synergetic or antagonistic effects on children’s immune systems. For instance, children coinfected with hookworm and Trichuris have been shown to be more likely to have blood hemoglobin levels indicative of anemia than children harboring only one of these parasites [30]. Furthermore, coinfection may create opportunities for viral and bacterial infections among the children as the immune systems of the children may reduce due to intestinal parasitic (protozoa and helminths) infection.

In this study, females were found to be heavily infected by more than one parasite as compared to males. This is in agreement with a study conducted by Asa et al. [31], where double and triple infections were common and more prevalent among females. The overall prevalence of parasite infection was found to be significant between females and males of malnourished children. In addition, this study investigated the trends of parasitic infection based on the study participants’ gender among the malnourished children. Thus, the study indicated a higher prevalence of parasitic infection in females, showing statistically significant variation as compared to the males (37% vs. 56%). This does not agree with a study in Iran [25] and in some studies in Ethiopia [22] that reported a higher prevalence of IPIs among males. However, this result was similar to the results from a study carried out in the southwest of Ethiopia, where the prevalence rate in females was slightly higher than in males [10]. The difference might be associated with the overall performance and/or activities performed by males and females in the country. In Ethiopia, male children are not mostly involved in caring for their elders and keeping, washing, and changing clothes (diapers). In addition, male children are not forced to clean houses and compounds and wash any dirty materials and baby’s clothes. So this might be the cause for the reduction of parasite infection in males as compared to females in this study.

The significant risk factors (p < 0.05) for IPIs in this study were HT, not WHWSAT, having CWA, and PWMS. The absence of or not using toilets is believed to expose individuals to parasite infection. Open-air defecation is strongly associated with IPIs [28]. Similarly, studies have linked open-field defecation to the spread of intestinal parasite diseases [32, 33], because helminth ova and intestinal protozoan cyst stages can survive for a long time. As a result, children can become infected through a variety of routes.

The age-wise analysis between age increment and parasite infection seems to have an inverse relation to each other. The overall infection observed was 46.24%, 39.78%, and 13.98% for the age groups of < 5, 6–10, and 11–14 years old, respectively. This indicates that the lower age groups were more susceptible and the higher age groups were less susceptible for parasitic infection among the malnourished children. The lower age groups (< 5 years old) mostly play with soil and dirty materials that are found in their area; especially in this age group, some may use diapers and put anything from their surroundings into their mouth. Therefore, this may increase the probability of being infected by any parasites that contaminate those materials. In addition, these age groups have less information about parasites, self-cleaning, and the risk of parasitic infection, and thus, they pay less attention to such conditions, unlike the higher age groups. The older children are more likely to practice better personal hygiene than the younger ones, especially in the presence of food shortages [34]. Young children and females in impoverished areas are particularly vulnerable due to underdeveloped immune systems, poor hygiene, and gender-specific roles that increase exposure to contaminated environments [25]. Furthermore, the double and triple infections were mainly observed in the middle-age (i.e., 6–10 years) groups. Children in this group have less maturity as compared to the last age group (i.e., 11–14 years) and spend their time outside of home paying less care for them. So this might be the cause of the increased occurrence of coinfection in this age group.

Child malnutrition, which includes both under- and overnutrition, is a global health issue. The three primary AIs used to measure child’s nutritional status are stunting, wasting, and underweight [35]. Underweight is a direct indicator of both chronic and acute malnutrition, since it represents both low height for age and low weight for age. Thus, in this study, we investigated the intensity of undernutrition among children based on three indicators (mild/slight, moderate, and severe). According to these indicators, 53.08% and 3.31% were mild/slight and severe, respectively. This may indicate that most of the children studied were lightly/mildly malnourished, and few of them were severely malnourished.

7. Conclusion

IPIs in this study area showed a high prevalence of 31.75% in malnourished children aged < 14 years, which is significantly higher than well-nourished children. The infection was high in females, unlike in males of malnourished children. In addition, no toilet usage, not WHWSAT, having CWA, and PWMS were found to be significant risk factors (p < 0.05) for IPIs in malnourished children. Hence, awareness-creation training should be given to Bele Gesgar areas to minimize parasite infections, and health offices should pay attention on the proper preparation and utilization of toilets. Parents should follow and take care of their children while they are staying out of home.

Ethics Statement

Ethical clearance and permission were obtained from Madda Walabu University, College of Health Science, and Goba Referral Hospital (Reference number: RMWU/14/131/542), and written consent was obtained from the study participants during stool sample collection.

Conflicts of Interest

The authors declare no conflicts of interests.

Author Contributions

D.A. designed the study, performed the statistical analysis, wrote the protocol and the first draft of the manuscript, and managed the literature searches. Z.F. managed the analyses of the study. All authors read and approved the final manuscript.

Funding

This study obtained no funding.