Burden of Enterobiasis in Africa: Overcoming Neglect and Improving Pediatric Health

Abstract

Enterobiasis is a globally prevalent, difficult-to-control, but yet neglected intestinal helminthiasis, with approximately 45% of the African pediatric population affected. Its asymptomatic nature in most cases leads to underestimation of its impact. However, its impact on pediatric health is significant, compromising their physical and mental well-being ultimately hampering educational development. The prevalence of enterobiasis among (pre)school-aged children in Africa may be higher than reported, but this depends on prioritizing and harnessing the scotch tape technique in epidemiological studies and routine parasitological examinations due to its high diagnostic efficiency. Mebendazole (100 mg orally) is the recommended first-line treatment, and administering a second dose after 14 days is crucial to prevent reinfection. The scarcity of treatment data for enterobiasis in Africa can be attributed to various factors, including underreporting of cases, limited healthcare infrastructure, and inadequate research focus on this specific parasitic infection. Overcoming the neglect of enterobiasis requires the implementation of educational and mass treatment programs, improving diagnostic capabilities, and prioritizing research and public health initiatives. Additionally, improving hygiene practices and sanitation is essential. By addressing these challenges and introducing comprehensive interventions, the neglect of enterobiasis can be overcome, leading to improved overall African pediatric well-being.

1. Introduction

Despite advancements in healthcare, parasitic diseases continue to pose a significant global public health challenge, particularly in developing countries where besides unmet healthcare needs, risk factors for parasite transmission remain persistent [1, 2, 3, 4, 5]. Caused by the nematode, Enterobius vermicularis (pinworm), enterobiasis is the most prevalent helminth infection, affecting an estimated 4–28% of children and more than 1 billion people globally [6]. This parasite has coexisted with humans since ancient times and continues to persist in modern populations [7]. Enterobiasis is often considered a relatively mild condition characterized symptomatically by perianal pruritus (itching). While most cases are asymptomatic, rare complications have been reported [5, 8, 9, 10, 11, 12, 13, 14].

Enterobiasis is often neglected in terms of public health recognition and research funding, leading to underestimation of its burden, particularly in Africa, where parasitic diseases are highly prevalent [1, 2]. Enterobiasis is frequently underestimated in comparison to other intestinal helminths, primarily due to the absence of apparent symptoms in most cases. Additionally, factors like the nocturnal migration of the parasites and the difficulties in detecting their eggs in routine stool examinations contribute to the underestimation of the disease burden [15]. However, untreated or under-treated enterobiasis can have long-term consequences on pediatric health, including impaired growth, nutritional deficiencies, impaired cognitive development, and compromised educational attainment [16, 17, 18, 19].

This chapter aims to highlight the burden of enterobiasis in Africa, emphasizing the need for prioritized efforts to improve pediatric health through comprehensive control measures. By doing so, the neglect of enterobiasis can be overcome, and the well-being of African pediatric populations improved.

2. Epidemiology of enterobiasis among African children: the need for more epidemiological data

Dependent on several factors including socio-demographic and economic status, hygienic factors, and diagnostic technique, the epidemiology of enterobiasis differs across different African countries and has been poorly mapped, contributing to the underestimation of the disease’s true burden in the region. However, available studies highlight the persistence of enterobiasis in African countries, with possible risk factors.

A study in rural coastal Tanzania showed higher prevalence rates of pinworm infection among preschool and school-aged children compared to infants [20]. The prevalence of pinworm infection varies in different studies, ranging from as low as 0.01% to as high as 45.3% in school-aged children [20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35]. These variations are attributed mainly to differences in diagnostic techniques, with studies using scotch tape reporting higher prevalences than those using fecal analysis.

Studies have highlighted the role of the infected hand in pinworm transmission among the pediatric population, with a high prevalence of pinworm eggs found on the hands and underneath the fingernails of school children [36, 37, 38, 39, 40]. These studies highlight the need for improved sanitation and proper handwashing with soap in schools to prevent parasite transmission. Overcrowded living conditions have been also associated with higher prevalence rates of pinworm infection, emphasizing the importance of addressing population density in prevention efforts [41]. Environmental factors, such as temperature, may also impact the transmission and survival of pinworm eggs [20].

Street food consumers and individuals who consume raw vegetables in Africa, particularly in sub-Saharan Africa (SSA), are identified as high-risk populations for pinworm infection. Studies conducted in Ghana and Nigeria have shown the association of pinworms with food vendors/handlers and the presence of pinworms in raw vegetables sold by market vendors [42, 43, 44]. Additionally, asymptomatic migrants from developing countries may carry pinworms, as demonstrated by screening studies on sub-Saharan African and Latin American immigrants [45].

It is important to note that the true prevalence of enterobiasis in Africa may be higher than reported due to underdiagnosis and limited surveillance systems. Other parasitic diseases such as malaria and schistosomiasis, due to their significant public health impact in Africa, may divert attention and resources away from enterobiasis surveillance and control efforts [23, 24, 34, 46, 47].

3. Impact of enterobiasis on pediatric health

The weakened immune system of children makes them vulnerable to intestinal parasitic infections (IPIs). This often leads to detrimental effects on their physical and intellectual well-being. However, the impact of IPIs on pediatric health depends on the parasite species, parasitemia and course of infection, and nutritional and immunological status of children [48].

While enterobiasis is generally asymptomatic, symptomatic cases are characterized by nocturnal perianal pruritus, which can lead to auto-infection as patients inadvertently transfer eggs under their fingernails. This itching can cause discomfort, insomnia, restlessness, and daytime drowsiness, particularly in children. Secondary lesions, such as mechanical dermatitis, can develop in the perianal or vulvar areas [49].

Although rare, complications of enterobiasis include parasites invading the reproductive organs, peritoneal cavity [8, 12], leading to hepatic enterobiasis, and acute appendicitis [10, 14]. Ectopic movements of pinworms have been associated with recurrent urinary tract infections, potentially resulting in secondary gastrointestinal infections [1]. The presence of a large number of adult worms in the bowel can cause additional symptoms like abdominal pain, tenesmus, constipation, and vaginitis [9, 13, 49].

In addition to the its impact on physical well-being, enterobiasis can also hamper a child’s cognitive, emotional, and educational development. Untreated and under-treated enterobiasis may result in growth retardation and insomnia, which subsequently contributes to attention deficits, learning disabilities, increased school absenteeism, and higher dropout rates [16, 19, 50]. For instance, after a night of deprived sleep resulting from perianal pruritus, children become fatigued and less active the next day, impacting their concentration and performance at school. Others may miss school not only as a result of fatigue but also to avoid stigmatization by peers.

4. Diagnosis of enterobiasis: prioritizing the scotch tape method

Accurate diagnosis of enterobiasis is crucial for estimating the disease’ burden, and disease management [51]. However, in Africa, diagnosis of intestinal helminthiasis is influenced by multiple factors including healthcare accessibility, educational status, and sociocultural beliefs.

Enterobiasis can be diagnosed by symptoms such as perianal pruritus, visual examination of adult worms, and microscopic examination of eggs and adult worms [50]. However, in Africa, most cases are asymptomatic, making diagnosis challenging and leading to an underestimation of the disease burden [52]. Diagnostic resources for pinworm infection in Africa are limited, and different methods have varying levels of effectiveness.

Stool microscopy, commonly used in clinical practice and prevalence studies in Africa, is not reliable for identifying E. vermicularis. It underestimates the prevalence and may miss treatable cases, especially among asymptomatic individuals with low parasitemia. Scotch tape microscopy effectively detects pinworm eggs, while stool microscopy is less reliable due to the stickiness of the eggs, causing them to adhere to the perianal skin and clothes [15, 21].

A study in Ethiopia found various intestinal helminths but no E. vermicularis parasites using fecal analysis [53]. Meanwhile, a study in Tanzania demonstrated reasonable prevalence of E. vermicularis, particularly among preschool-aged children, using scotch tape microscopy for E. vermicularis detection in combination with stool microscopy for other helminths [20]. Likewise, a study in South Africa showed higher pinworm prevalence using scotch tape microscopy among hospitalized children compared to stool microscopy among school-going children [21]. This highlights the underestimation of pinworm prevalence by stool microscopy and emphasizes the importance of scotch tape microscopy in diagnosing and studying pinworm infection in Africa.

Serological methods are of no relevance for diagnosing pinworm infections. However, PCR is a highly precise tool for diagnosing intestinal helminth infections [54, 55]. A study proposed a PCR-based method for E. vermicularis diagnosis, and its high diagnostic accuracy can address and overcome the challenges posed by other methods [56]. In resource-limited settings, however, this approach may be impractical to use particularly in smaller laboratories located at the periphery [55].

The Scotch tape method for diagnosing pinworm infection is thus crucial and should be prioritized, particularly in resource-limited settings in Africa. Although the collection method may be unpleasant and cumbersome for some individuals, the advantages of this diagnostic approach such as its ease of use, rapid results, cost effectiveness, and high sensitivity make it valuable. Furthermore, the implementation of the Scotch tape method in E. vermicularis epidemiological studies has the potential to estimate the true burden of the disease in Africa.

5. Treatment of enterobiasis in Africa

Enterobiasis can be effectively treated using highly effective anthelminthic drugs. Initial treatment of enterobiasis may not provide complete protection as reinfection is common [20]. It is recommended to treat enterobiasis with a single dose of albendazole (400 mg orally), mebendazole (100 mg orally), or pyrantel pamoate (11 mg/kg orally). To target newly developed adult worms and prevent reinfection, a second dose should be administered 14 days later [57]. However, mebendazole is the first-line treatment for enterobiasis [50].

The available literature and research on the specific treatment outcomes, efficacy, and prevalence of drug resistance for E. vermicularis in African populations are limited [58]. Anthelmintic drug resistance has been highlighted in studies worldwide [59], but resistance of E. vermicularis to anthelminthic drugs have been poorly explored. Given the indiscriminate use of antimicrobials and practice of self-medication in several African countries, resistance patterns are frequent [60], but it is unknown whether resistance patterns of E. vermicularis are significant.

The scarcity of treatment data for enterobiasis in Africa may be attributed to various factors, including underreporting of cases, limited healthcare infrastructure, and inadequate research focus on this specific parasitic infection. Limited availability and utilization of standard diagnostics in routine parasitological examinations contribute to the lack of comprehensive treatment data for enterobiasis in Africa. The scotch tape test, the most effective for diagnosing enterobiasis, is less frequently employed in clinical parasitological examinations. As a result, many cases of the infection, particularly asymptomatic ones, may go undiagnosed and unreported. This underreporting further hampers the collection of accurate treatment data, making it difficult to assess the true burden and impact of enterobiasis in Africa.

Moreover, the limited healthcare infrastructure in rural areas worsens the challenges in diagnosing and treating enterobiasis. In these resource-constrained settings, the availability of healthcare facilities, trained personnel, and access to medications is inadequate. As a result, infected children who seek medical attention for symptomatic infections may face obstacles in receiving appropriate treatment. This lack of access to treatment contributes to the scarcity of treatment data and hinders the surveillance of treatment efficacy.

Conducting large-scale clinical trials and monitoring treatment outcomes in resource-limited settings can be logistically challenging [61]. Limited funding, inadequate research infrastructure, and difficulties in follow-up and data collection pose significant barriers to conducting comprehensive studies on enterobiasis treatment in Africa. These challenges further impede the generation of robust treatment data that could inform evidence-based guidelines and interventions.

6. Overcoming neglect: strategies for improved pediatric health

To mitigate the impact of enterobiasis on pediatric health in Africa, interventions are needed at both individual and community levels. These interventions should focus on improving sanitation facilities, promoting proper hygiene practices, providing access to effective treatment, and raising awareness about the importance of prevention and control measures.

Studies reporting high prevalence have highlighted that mass treatment and educational programs should be undertaken, to reduce enterobiasis reinfection and new infections to people in endemic areas [62, 63]. Furthermore, hygienic measures should be prioritized to help reduce the transmission of the parasite [39, 44, 64].

Addressing the epidemiology of enterobiasis in Africa requires the need for continuous epidemiological research [65]. These studies should utilize sensitive diagnostic methods particularly the scotch tape method to accurately determine the prevalence and distribution of enterobiasis. Moreover, the scotch tape method should be employed in routine parasitological examinations to diagnose infections accurately.

7. Conclusion and future directions

Enterobiasis, with a reported prevalence of approximately 45% in Africa, is a significant yet neglected helminth infection that primarily affects children. The lack of apparent symptoms has led to the underestimation of its disease burden. However, the high prevalence of risk factors such as poor hygiene, consumption of contaminated food, and overcrowding in African countries poses a serious threat to children, particularly those in rural areas.

Traditional diagnostic methods like stool microscopy have proven ineffective in diagnosing enterobiasis due to the stickiness of the eggs, necessitating the use of the scotch tape technique, which yields higher parasitemia. Treatment should prioritize preventing reinfection by administering the recommended dose of albendazole, mebendazole, or pyrantel pamoate, with a second dose after 14 days. To overcome the neglect of enterobiasis, two key interventions are required: mass treatment and education programs. Moreover, improving sanitation facilities, and practicing proper hygiene are important preventive and control measures.

It is crucial to allocate resources and prioritize research efforts toward studies specifically focused on E. vermicularis in African pediatric populations. These studies should aim to gather more epidemiological and treatment data, including prevalence, transmission dynamics, treatment outcomes, and potential drug resistance patterns. By addressing these research gaps, we can better understand and combat enterobiasis in Africa, thus improving the health and well-being of affected children.

Conflict of interest

The authors declare no conflict of interest.