Helminthiasis in school-age children from Gresik, East Java, Indonesia

Soil-transmitted helminths are the most common infections that can decrease children’s productivity. Around 1.5 billion people globally (24 % of the world’s population) were infected with helminths. Helminthiasis frequently occurs in regions with poor hygiene and limited access to clean water, sanitation, and hygiene in tropical and subtropical areas. The number of helminthiases was highest in sub-Saharan Africa, followed by China, South America, and Asia. Helminthiasis is transmitted by helminth eggs, which can be found in human feces. Then, it can contaminate the soil around human habitat. The current data shows that helminths infected more than 260 million preschool-age children, and the highest group is school-age children, with the number of 654 million (WHO, 2022).

Some helminth groups include Ascaris lumbricoides, Trichuris trichiura, Enterobius vermicularis, Necator americanus, and Ancylostoma duodenale. The three species that cause schistosomiasis in the latter group are Schistosoma mansoni, Schistosoma haematobium, and Schistosoma japonicum (CDC, 2023).

Helminthiasis can have various impacts on children and pregnant women. Expectant mothers and fetuses are at risk due to iron deficiency anemia, which is brought on by chronic blood loss and iron store depletion caused by hookworms (Degarege et al., 2022). Iron deficiency anemia and intestinal ulceration result from trichuriasis (Pabalan et al., 2018). Additionally, children’s learning, memory, and intelligence deficiencies may result from STH and schistosomiasis (Pabalan et al., 2018).

The outcomes of STH infection may be more severe, especially in immunocompromised children or adults. Iron deficiency and other micronutrients are two long-term impacts of helminthiasis that have been associated, specifically in school-age children (Gitore et al., 2020). Previous studies show that helminthiasis is associated with higher stunting rates, impaired cognition, low productivity, and low academic performance (Pabalan et al., 2018). Some risk factors of helminthiasis have been reported, such as insufficient water supply, poor hygiene practices, low socioeconomic status, living near animals, and living in urban areas (Chopra et al., 2022). Soil-transmitted helminths (STHs) include intestinal nematodes such as Ascaris lumbricoides, Trichuris trichiura, and hookworms (Necator americanus and Ancylostoma duodenale) that infect humans (Weaver et al., 2010; De Silva et al., 2014). Helminthiasis was classified as one of the neglected tropical diseases by the World Health Organization. Asia accounted for the significant burden of infections, with at least 25 % (26.4 %) of the population believed to harbor at least one STH species (Pullan et al., 2014). Numerous detrimental health effects, including diarrhea, malnutrition, and delayed physical and mental development, can be brought on by STHs. The most severe infections have the most noticeable effects on a child’s growth, but mild infections can also cause deficiencies in growth if the community’s nutritional status is subpar (Stephenson et al., 2000; Okyay et al., 2004).

According to the World Health Organization (WHO), regular schoolbased targeted preventive chemotherapy (PC) using albendazole or mebendazole for preschool- and school-aged children is the primary strategy to achieve STH controls (WHO, 2022). The most recent road map for non-communicable diseases (NDDs) released by the WHO aims to eradicate STHs as a public health issue in 96 % of endemic countries by 2030. The definition of elimination as a public health issue is <2 % prevalence of moderate-to-heavy STH infections (Casulli et al., 2021).

Gresik is one of the regions in East Java, Indonesia, that frequently experiences flooding, which can lead to poor hygiene practices. Laboratory examinations are required regularly to diagnose most parasitic diseases, as physical examinations alone are insufficient. This study aims to investigate the occurrence of helminth infection in school-age children in Gresik, East Java, Indonesia.

Our study design was approved by the Ethical Committee of Ibnu Sina Gresik Hospital, which has the registered number 071/066/437.76/2023.

Our study shows that Ascaris lumbricoides was the most common helminth infection found in school-age children in Gresik Regency (7.1 %). This result was in line with other published studies. Ascariasis is a prevalent public health issue among school-age children in developing nations, as reported in Pakistan. A study in Pakistan shows the prevalence of Ascaris infection was 0.88 % (Ali et al., 2020). Ascaris lumbricoides is known as the helminth larvae, which can migrate to the human body, such as to the lungs, leading to some clinical manifestations. Severely infected children can experience volvulus, intestinal obstruction, and intestinal necrosis (Zheng et al., 2012). A cross-sectional study in Nusa Tenggara, Indonesia, also reveals that Ascaris lumbricoides was the most common cause of helminth infection in school-age children, with a prevalence of 6.25 % (Bria et al., 2022).

Parasitic disease, especially helminthiasis, has still become a major public health problem in developing countries, including Indonesia. Sociodemographic factors play an important role and are associated with the incidence of helminthiasis. The detail of the demographic factors can be shown in Table 3. As revealed by another study in Nigeria (Chukuwuma et al., 2009), Pakistan (Hussain et al., 2011), and Khamir (Rather & Salati., 2010) showed that poor personal hygiene, low socioeconomic status, insufficient clean water supply, poor sewage system, and low levels of sanitary settings were significantly associated with the helminthiasis. Some stray animals (cats and dogs) closest to humans must also be considered a source of Ascaris lumbricoides egg transmission (Olayide et al., 2008). For example, a cross-sectional study in Bali revealed dogs’ role as transmitters of Ascariasis. The fecal sample from the dog shows the diversity of helminth eggs, including Ancylostoma sp., Ascaris sp., and Trichuris sp (Agustina et al., 2021). This present study shows that the percentage of some risk factors of STHs among school-age children is still high, where removal of shoes while playing in the yard, playing in the dumpsite, not washing hands before eating, defecation while in school, and not washing of hand with soap after defecation are high-risk factors. According to another report, children are more likely than adults to walk barefoot, increasing their contact with the ground and disregard sanitary facilities even when available (Abera et al., 2013). Our study also showed that unwashed hands with soap after defecation is the risk factor for helminthiasis. This was also confirmed by another study from Iran (Daryani et al., 2012), Uzbekistan (Gungroen et al., 2007), China (Balen et al., 2011), India (Kaliappan et al., 2013; Awasthi et al., 2008), and Nepal (Tandukar et al., 2013). It is estimated that Trichuris trichiura infects 465 million people globally, according to recent estimates. Humans infected with Trichuris trichiura are known to experience adverse health outcomes, and most of these individuals are children (Dunn et al., 2016; Cruz et al., 2021). Trichuris trichiura is the STH helminth parasite linked to stunting and wasting in children who unexpectedly ingest the Trichuris egg from water or contaminated food (Else et al., 2020). Trichuris infection commonly infects children, leading to malnourishment, anemia, stunting, and other nutritional deficiencies (Stephenson et al., 2000). Although low-intensity infections involving multiple parasite species can cause significant anemia, light single Trichuris trichiura infections are considered relatively benign (Ezeamama et al., 2005). This study also found that Trichuris infection prevalence was at 1.63 %. It is much lower than that shown in another cross-sectional study in Thailand, which was 2.1 % (Kache et al., 2020).

Helminth infection in school-age children can influence their school performance. Previous studies show that children with hookworm infection perform worse in school. The previous semester’s average for children with hookworm infection was 67.26, while the average for children without hookworm infection was 69.76. Two independent sample t-tests confirmed these results to be statistically significant. This results from hookworm’s impact on brain cell development and cognitive function (Feleke et al., 2018).

In our study, female and male genders show a proportional percentage, showing the same prevalence. This data contrasts with the other study in Nusa Tenggara, which shows female students were more frequently infected than male students (Bria et al., 2022). Another study shows that soil-transmitted helminths can occur in pregnant women (SHIP), which may contribute to the emotional development of sixth-year-old children (Garrison et al., 2021). Another study shows no significant correlation between sex and helminth infection in Southeast Nigeria (Uneke et al., 2007). However, it is at odds with findings regarding intestinal helminthiasis among students in Ilie, Osun State, Southwest Nigeria (Adefioye et al., 2011), where there is a significant difference in the percentages of male and female pupils infected. The relationship between helminth infection and sex has not yet been determined, though some studies have suggested that it is (Aiwo et al., 2000), while others have suggested otherwise (Uneke et al., 2007). Therefore, more thorough research is still required to understand this matter fully (Narain et al., 2000).

Twenty-two feces from 183 children tested positive for helminth eggs, including 14 children infected by Ascaris lumbricoides (6.36 %), 3 children infected by Trichuris trichiura (1.304 %), 3 children infected by Oxyuris vermicularis (1.304 %), and 3 children infected by Hookworm (1.304 %). The highest prevalence was found in 7-year-old children (31.8 %).