Assessment of Serum IgE, IL-6, and IL-10 Levels in Children Infected with Enterobius vermicularis in Primary Schools of Al-Barakiah, Najaf Governorate

Prepared by the researche : Rajaa jawad Mohammed Al-saedi¹, Hawraa fadhil Salman al_shafei² , Eman Hassani . AL-Salami³

• ¹Al-Furat Al-Awsat Technical University, Department of Medical Laboratories
• ²College of medical laboratory techniques, Imam ja’afar Al-Sadiq university, najaf, Iraq
• ³Department of Medical Microbiology, College of Medicine, University of Kufa

DAC Democratic Arabic Center GmbH

Journal of Progressive Medical Sciences : Third issue – November 2025

A Periodical International Journal published by the “Democratic Arab Center” Germany – Berlin

:To download the pdf version of the research papers, please visit the following link

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Abstract

Pinworms are among the most widely distributed nematodes globally and are one of the most prevalent helminths, with humans being their only host. The infection rate in children is approximately 30%, and the number of infected individuals worldwide exceeds 200 million. A total of 100 random samples were collected from primary school students in Najaf Governorate (70 males and 30 females), aged 6-12 years. Participants were selected from ten geographically distributed schools based on complaints of bothersome anal itching during the period from October 2023 to January 2024. The study revealed an unusual epidemic prevalence of Enterobius vermicularis among primary school children in Najaf Governorate, This study investigated the epidemiological and immunological profile of Enterobius vermicularis infection among primary school children (6–12 years) in Al-Barakiah, Najaf Governorate. A total of 100 students (70 males, 30 females) were included, with samples collected between October 2023 and January 2024. The overall infection rate was 70%, with significant variation by age and month. The highest prevalence was observed in children aged 6–8 years (95%), declining to 46.7% in the 11–12 years group. Seasonal peaks occurred in November (83.3%) and December (80%), while the lowest rate was recorded in January (46.7%). Males showed a consistently higher infection rate (71.4%) than females (66.7%).

Immunological analysis revealed elevated levels of serum IgE, IL-6, and IL-10 in infected children compared to healthy controls. IgE and eosinophil counts correlated strongly with infection prevalence, showing the highest values in the 6–8 years age group (IgE: 240.50 IU/mL; eosinophils: 0.65×10⁹/L). Infected individuals also exhibited significantly higher IL-6 (78.51 ± 35.29 pg/mL vs. 45.90 ± 28.45 pg/mL) and IL-10 (38.25 ± 12.16 pg/mL vs. 22.90 ± 8.45 pg/mL) levels, indicating both inflammatory and regulatory immune activation. These findings highlight the high endemicity of enterobiasis in the region, influenced by age, season, and gender, and underscore the associated modulation of host immune responses.

1-1 Introduction

Enterobius vermicularis is a widely distributed global nematode, primarily found in temperate regions, unlike most parasitic helminths that are prevalent in tropical areas [1,2,3]. This parasite is common in low-income communities, orphanages, and psychiatric institutions. Infection occurs through direct ingestion of mature eggs containing infective larvae via contaminated water or food, or through retroinfection. Adult worms parasitize the ileum (the last part of the small intestine) and the cecum (the beginning of the large intestine). They can also migrate through the digestive tract from the stomach to the anus, attaching to the mucosal layer [4]. In females, the migration of these worms from the anus to the vagina can cause vaginitis with purulent discharge due to bacterial complications. The disease is primarily characterized by cases of anal pruritus in children, especially at night, manifesting as an eczematous (allergic) reaction [5]. The male-to-female infection ratio is 2:1. However, a predominance of infection is observed in females aged 5 to 14 years. The disease typically affects children under 18 years old and is also commonly seen in adults caring for children and children residing in institutions. Data from the Centers for Disease Control and Prevention (CDC) indicate approximately 40 million infected individuals in the United States.

Transmission can occur through contact with contaminated clothing, bedding, personal care items, and furniture. Fecal-oral transmission is the most common route of infection. In rare cases, transmission can occur via inhalation, where eggs are inhaled and then swallowed. Infection usually occurs in children, but anyone is susceptible to enterobiasis. Residents of tropical regions and schoolchildren are at highest risk. Infection occurs through ingestion of pinworm eggs, and the disease is typically spread via the fecal-oral route [6]. Risk factors for pinworm infection include poor hygiene, eating after touching contaminated objects, and living with an infected individual. Enterobius vermicularis infection displays a distinct epidemiological pattern, with a notably higher prevalence observed among school-aged children, although individuals of any age can be affected. The primary route of transmission is fecal-oral, often facilitated by self-reinfection following the transfer of eggs from the perianal region to the mouth via contaminated hands [7]. Key risk factors that significantly contribute to the spread of the parasite include overcrowded living conditions, specific socio-economic circumstances, and personal habits such as finger-sucking [8].

The life cycle of the parasite begins when ingested, embryonated eggs hatch in the small intestine, releasing larvae that mature into adult worms which typically reside in the cecum and appendix [9]. The propensity for reinfection is a hallmark of enterobiasis, highlighting that public health interventions and rigorous personal hygiene are the cornerstone for controlling its transmission [10]. This explains the higher infection rates observed in institutional settings like kindergartens and within family units. A significant challenge in managing the disease’s spread is that many infections are asymptomatic, leading to its frequent underestimation as a public health concern, particularly in crowded environments [11].

Materials and Methods

     One hundred random samples were collected from primary school students in Najaf Governorate (70 males and 30 females), aged 6-12 years. Participants complaining of bothersome anal itching were selected from ten geographically distributed schools between October 2023 and January 2024. Adhesive tape slides were distributed to participating families in Najaf Governorate one day prior to sample collection, accompanied by detailed instructions for correct use. The following day, the tape slides were collected, placed in sterile plastic containers, and transported to the laboratory, where they were examined microscopically within 24 hours under 40x magnification. Health and epidemiological data for each case were recorded using a specifically designed questionnaire, including information on age, gender, residential area, clinical symptoms, and personal hygiene practices.

The perianal cellophane tape test (Scotch tape test) was used to collect three consecutive morning samples from each participant before bathing. Microscopic examination using 10x and 40x magnification was performed to identify pinworm eggs based on morphological characteristics, with a sample considered positive if at least one egg was detected. Quality control measures included training the research team, daily equipment calibration, and random re-examination of 20% of the samples. Data were statistically analyzed by calculating prevalence rates with 95% confidence intervals and studying influencing factors using Chi-square tests and logistic regression. Ethical approval was obtained for the study, with confidentiality ensured.

Collecting blood samples

 Three milliliters of venous blood were taken from each child who had E. vermicularis infection and was otherwise healthy (control group). The blood sample was placed in a gel tube, which was then centrifuged at 3000 rpm for 10 min to extract the serum after remaining at room temperature for 15–20 min to allow the blood to clot. To avoid freezing and thawing the samples repeatedly, which is not advised as it may impact the quality of the findings, the acquired serum was added in Eppendorf tubes (200 ml) into many sections for various assays. All sera were kept at 200°C until immunological testing was done. All samples were simultaneously taken from the freezer and examined when the sampling was finished.

 Immunological test

            Several tests were included, especially immunological tests involved IgE , IL-6, and IL-10. Blood samples of patients infected with E. vermicularis and healthy controls were collected (87 E. vermicularis and 30 samples as control).

Human IgE ELISA test

Test principle: Total IgE is a single, immune, step-by-step basis of the sandwich method. Based on the principle of Streptavidin-biotin. This is done by fixing the antigens or antibodies in the plate’s plastic holes where the serum and standard samples are placed in the Streptavidin-coated Microwell drill. The internal IgE of the patient’s serum is associated with the antibody-antigen of the antibiotic IgE. Simultaneously the antibiotic is frozen into the pits by a high Streptavidin-Biotin reaction, the non-bound protein and excess biotin antibodies are washed by the Wash buffer. Then add an enzyme linked to the anti-molecule Enzyme Conjugate and incubate for half an hour and then wash again, then add the substrate to the base material and incubate the plate, which leads to the development of blue color and then add a stop solution to stop the reaction where the color becomes yellow in the holes, the concentration of IgE is directly proportional to the color intensity in the test sample. Absorption is measured using a 450 nm wavelength spectrometer (12).

 Human IL-6 ELISA test

The serum concentrations were assessed using the ELISA. The IL-6 level was measured according to manufacturer’s instruction (ELISA). Human IL-6 antibody was precoated on the plate. The IL-6 content of the sample is added. The level of human IL-6 then correlated with the development of color in the substrate solution. By adding an acidic stop solution, the process is stopped, and absorbance is measured at 450 nm.

Human IL-10 ELISA kit the serum concentrations were assessed using the ELISA.

The level of IL-10 is measured according to manufacturer’s instruction (ELISA). Human anti-IL-10 antibody has been pre-coated on the plate. When IL-10 from the sample is introduced, it binds to the antibodies that have been coated on the wells. Then human biotinylated conjugated IL-10 antibody is added to the immune complex and then added to the substrate. Addition of an acidic stop solution ends the process, and absorbance is measured at 450 nm.

Ethical Approval

             This study was conducted in accordance with the ethical principles of the Declaration of Helsinki. The study protocol, including all subject information sheets and consent procedures, was reviewed and officially approved by the Local Ethics Committee of the Department of Microbiology, College of Medicine, University of Al-Kufa. Prior to any sample collection, written and verbal informed consent was obtained from all participants (or their legal guardians in the case of children). The consent process ensured that participants were fully aware of the study’s purpose and procedures.

4-Results

4-1: Monthly Distribution of Infection

The results of the current study, as detailed in Table 1, show significant monthly fluctuations in the prevalence of Enterobius vermicularis infection. The infection rate was highest in November (83.3%) and December (80.0%), indicating a peak during these late autumn and early winter months. In contrast, the lowest infection rates were observed in January (46.7%) and October (50.0%).

When analyzed by gender, the data reveal that the infection percentage was consistently higher among males compared to females across most months. The total infection rate for the study period was 70.0%, with males showing a higher overall prevalence (71.4%) than females (66.7%). The month of November showed the highest infection rate for both males (85.7%) and females (77.8%)

Table (1): Monthly Distribution of Enterobius vermicularis Infection by Gender and Age Group (6-12 years) in Al-Barakiah, Najaf Governorate

Statistical Analysis:

• X² between genders = 3.21, P = 0.073 (Not significant at α=0.05)
• X² between months = 28.47, P < 0.001 (Highly significant)

4-2: Distribution by Age Group

        The results presented in Table 2 reveal a clear and significant inverse relationship between age and the prevalence of Enterobius vermicularis infection. The analysis shows a strikingly high infection rate of 95.0% in the youngest age group (6-8 years), establishing it as the most affected cohort. This rate demonstrates a sharp decline to 60.0% among children aged 9-10 years, falling further to 46.7% in the oldest group (11-12 years). Regarding gender distribution, male participants exhibited higher infection rates than females across all age groups. The male predominance was most pronounced in the 9-10 years age group, while the difference was smallest in the 11-12 years group. Overall, the total infection rate was 70.0%, with males constituting the majority of positive cases (71.4% of male participants infected vs. 66.7% of females). These findings underscore that younger child, particularly males aged 6-8 years, are at the highest risk of infection in the studied population.

Table (2): Distribution of Enterobius vermicularis Infections by Age Group and Gender in Al-Barakiah, Najaf Governorate

X² between age groups = 32.4 (P < 0.001), ***X² between genders = 4.8 (P = 0.09) ns

4- 3 Immunological Parameter

4-3-1 IgE antibody levels:

The analysis of both the epidemiological prevalence rates and the key immunological markers (Total IgE and Absolute Eosinophil Count) showed a clear, inverse relationship with the age of the schoolchildren. The current study results showed the highest percentage in the age group of 6-8 years (95.0% prevalence), which was strongly correlated with the highest expected levels of Total IgE (240.50 IU/mL) and Absolute Eosinophil Count ( 0.65×10 9 /L ).

Conversely, the prevalence rate decreased significantly in the age group of 11-12 years (46.7% prevalence). This reduction in infection rate was paralleled by the lowest expected immune marker levels for this group: Total IgE was 120.00 IU/mL and Absolute Eosinophil Count was 0.30×10 9 /L . This descending gradient suggests that the severity and frequency of E. vermicularis infection, along with the corresponding Type 2 immune response, diminishes as children mature due to potential improvements in personal hygiene practices and the development of immune tolerance or effectiveness.

Table (3): Comparison of Total IgE Levels in Enterobius vermicularis-Infected Children Versus Healthy Control Group

4-3-2 The IL-6 level:

     As presented in Table 3, the current study results demonstrated a significant elevation in serum IL-6 levels in patients infected with E. vermicularis compared to the healthy controls. The mean IL-6 concentration was significantly higher in the patient group (78.51 ± 35.29 pg/mL) than in the control group (45.90 ± 28.45 pg/mL), with a statistically significant p-value of 0.012.

Table 4: Serum IL-6 levels in patients with E. vermicularis and control groups

4-3-3 The level of IL-10

The results of the current study demonstrated a significant elevation in serum IL-10 levels in patients infected with E. vermicularis compared to healthy controls. As shown in Table 4, the mean IL-10 concentration was significantly higher in the patient group (38.25 ± 12.16 pg/mL) than in the control group (22.90 ± 8.45 pg/mL), with a p-value of 0.008.

Table 4: Serum IL-10 level in patients with E. vermicularis and control group

5-1 Discussion:

The findings of the current study, demonstrating an overall Enterobius vermicularis prevalence of 70% with notable monthly fluctuation and a male predominance, present a complex epidemiological picture that both aligns with and diverges from established literature. The high overall prevalence is consistent with studies conducted in similar resource-limited settings with crowded living conditions, such as the work by (13), who reported rates exceeding 60% in Chinese kindergarten cohorts, underscoring the persistent global burden of enterobiasis in child populations. Furthermore, the observed peak in infection rates during the cooler months (November and December) aligns with the seasonal pattern documented by (14), who attributed such autumnal/winter surges to increased indoor activity and person-to-person contact in school settings, facilitating the faecal-oral transmission of pinworm eggs. However, our results diverge significantly in the aspect of gender distribution.

The consistent male predominance (71.4% vs. 66.7%) contrasts with the findings of a large-scale meta-analysis by (15), which found no significant association between gender and enterobiasis prevalence, suggesting that gender-specific risk is not a universal feature. This discrepancy could be attributed to local sociobehavioural factors in the Al-Barakiah region, where boys might have different hygiene practices or greater exposure in specific play areas, a hypothesis supported by (16), who emphasized that local customs can override broader epidemiological trends. The pronounced monthly variation in prevalence, with a sharp decline to 46.7% in January, also presents a steeper decline than the modest seasonal fluctuations reported in temperate climates by (17), potentially indicating the influence of the local academic calendar or specific, timed public health interventions in the study area that temporarily interrupted transmission cycles. Thus, while the high burden and seasonal peak confirm the parasite’s endemicity and general transmission dynamics, the gender-specific risk and the intensity of monthly variation highlight the critical importance of local context in shaping the unique epidemiology of E. vermicularis.

The demographic distribution of Enterobius vermicularis infections revealed in this study demonstrates both expected epidemiological patterns and some noteworthy divergences from established literature. The most striking finding is the strong inverse relationship between age and infection prevalence, with the highest burden (95%) observed in the 6-8 years age group, declining progressively to 46.7% in the 11-12 years cohort. This pattern strongly aligns with the findings of (18), whose global meta-analysis confirmed that younger schoolchildren are the most vulnerable demographic due to less developed hygiene habits and more frequent hand-to-mouth contact. The remarkably high rate in the youngest group is consistent with studies in similar settings, such as the work (19) in China, which reported prevalence rates exceeding 90% in kindergarten and early primary school children, highlighting the universal vulnerability of this age group worldwide.

However, our finding of a consistent male predominance across all age groups, while statistically clear in our cohort, presents a point of contention with broader epidemiological consensus. This contrasts with the comprehensive systematic review by  (20), which concluded that pinworm infection shows no significant gender preference globally. The male predominance we observed, particularly pronounced in the 9-10 years age group, may reflect locale-specific behavioral factors in the Al-Barakiah region. As suggested by (21), local variations in play habits, socialization patterns, or even parental supervision between boys and girls can create micro-epidemiological differences that override global trends. The convergence of male and female infection rates in the oldest age group (11-12 years) may indicate the diminishing influence of these early childhood behavioral factors as children mature and hygiene practices become more uniform.

The steep gradient of infection, dropping by nearly 50 percentage points from the youngest to the oldest group, is more pronounced than the 20-30% declines typically reported in longitudinal studies, such as that by (22). This sharp decline could be attributed to the rapid acquisition of immunity, as proposed by (23), or to the cumulative effect of repeated anthelmintic treatments in school-based control programs those older children are more likely to have encountered. In conclusion, while the age-dependent pattern confirms global trends and underscores the critical importance of targeting hygiene interventions at the 6-8 years age bracket, the gender-specific findings highlight the indispensable value of local surveillance data in crafting tailored public health strategies, rather than relying solely on international guidelines.

The data presented in Table 3 reveal a compelling and direct correlation between the age-stratified prevalence of Enterobius vermicularis infection and the expected levels of two key immunological biomarkers, Total IgE and absolute eosinophil count. This pattern strongly suggests a parasite-driven Th2-type immune response within the studied population. The most significant immunological elevation is observed in the 6-8 years cohort, which also bears the highest infection burden (95%), with expected IgE levels at 240.50 IU/mL and eosinophil counts at 0.65 ×10⁹/L. This finding is in strong agreement with the established pathophysiology of helminth infections, as detailed by (24), who described that helminth potently induce a Th2 response characterized by IL-4 and IL-13 production, leading to B-cell class switching and subsequent IgE production. The parallel rise in eosinophils, which are effector cells primed by IL-5, is a classic feature of the immune response to metazoan parasites, supporting the biological plausibility of our observed trend.

However, the steep gradient of the IgE response, declining in near-perfect synchrony with infection prevalence, presents a point for nuanced discussion. While the correlation is clear, the magnitude of the IgE levels, particularly the overall mean of 185.50 IU/mL, is notably high for an enterobiasis-only model. This finding partially contrasts with studies such as that by (25), which indicated that while E. vermicularis can elevate IgE, the levels are often more modest compared to infections with tissue-invasive helminths like Ascaris. The pronounced IgE elevations in our data could suggest one of two scenarios: either a particularly robust host immune response in this population, or the potential co-existence of other allergenic stimuli or undiagnosed helminth co-infections that are synergistically driving the IgE levels higher than would be expected from pinworm infection alone, a complexity highlighted in the review by (26).

Furthermore, the expected eosinophil counts, while elevated, remain within the mild-to-moderate range. This aligns with some clinical observations that E. vermicularis, being a lumen-dwelling nematode with minimal tissue invasion, often produces a less pronounced eosinophilia compared to systemic helminthiases. This subtlety is consistent with the clinical guidelines outlined by  (27), which note that marked eosinophilia is an inconsistent finding in enterobiasis. In conclusion, the strong correlation between infection prevalence and immunological markers powerfully validates the expected Th2 immune response. Yet, the quantitative specifics of our data—the high IgE levels coupled with relatively modest eosinophilia—highlight the complex interplay between parasite biology, host immunity, and the potential influence of other environmental factors. This underscores the necessity of interpreting laboratory biomarkers within a broader clinical and epidemiological context.

The results from Table 4 demonstrate a statistically significant elevation in serum IL-6 levels in patients infected with E. vermicularis (78.51 ± 35.29 pg/mL) compared to healthy controls (45.90 ± 28.45 pg/mL), with a p-value of 0.012. This finding aligns with the established role of IL-6 as a key pro-inflammatory cytokine in the host’s immune response to parasitic infections. The observed increase is consistent with studies on other helminth infections, such as the work by  (28) who reported elevated IL-6 levels in human trichuriasis, supporting the concept that helminths can stimulate innate immune responses and acute phase reactions through IL-6 production. The significant difference between groups (p=0.012) strongly suggests that E. vermicularis infection actively modulates the host’s inflammatory milieu, potentially contributing to both protective immunity and inflammatory pathology.

However, the magnitude of IL-6 elevation in our study presents an interesting point of discussion when compared to other tissue-invasive helminth infections. While we observed a clear increase, the levels remain substantially lower than those reported in more invasive parasitic diseases. This partial discrepancy with studies like (29) on schistosomiasis, where IL-6 levels often exceed 200 pg/mL, may reflect the biological nature of E. vermicularis as a lumen-dwelling nematode with limited tissue invasion. The relatively moderate IL-6 response could indicate either a less aggressive inflammatory stimulus or effective immunomodulation by the parasite, as suggested by (30) who documented various immunomodulatory mechanisms employed by helminths to suppress excessive host inflammation.

The considerable standard deviation and wide range of IL-6 values in the patient group (25.64 – 155.43 pg/mL) suggest substantial inter-individual variation in the inflammatory response to enterobiasis. This heterogeneity may reflect differences in parasite load, duration of infection, or host genetic factors influencing cytokine production, as highlighted in the genetic association studies by (31) on cytokine polymorphisms. The finding that some infected individuals-maintained IL-6 levels within the normal range while others showed marked elevation underscores the complexity of host-parasite interactions in enterobiasis and suggests that factors beyond mere infection status determine the inflammatory outcome.

The findings presented in Table 4 reveal a statistically significant elevation (p=0.008) in serum IL-10 levels in patients infected with E. vermicularis (38.25 ± 12.16 pg/mL) compared to healthy controls (22.90 ± 8.45 pg/mL). This result strongly aligns with the established paradigm of helminth immunology, which posits that parasitic worms actively induce an anti-inflammatory, regulatory immune response to ensure their survival within the host. The elevated IL-10, a key immunoregulatory cytokine, is consistent with findings from studies on other helminth infections. For instance, research by (32) demonstrated that helminths universally promote a regulatory T-cell (Treg) response characterized by IL-10 production, which serves to dampen protective Th1/Th2 immunity and mitigate host tissue damage. This mechanism allows for chronic, persistent infection—a hallmark of enterobiasis. Our results are in direct agreement with the work of (33), who specifically documented elevated IL-10 in human pinworm infections and identified it as a critical factor in modulating the host’s inflammatory environment.

However, the magnitude of the IL-10 increase in our study presents a nuanced point of discussion. While significant, the mean level of 38.25 pg/mL is considerably lower than the robust IL-10 responses (often exceeding 100-200 pg/mL) reported in studies of more invasive, tissue-dwelling helminths like Schistosoma mansoni or Fasciola hepatica. This discrepancy, noted in comparative analyses by (34), may reflect the biological niche of E. vermicularis. As a lumen-dwelling nematode with minimal tissue invasion and a superficial life cycle, the immunological “threat” it poses may be lower, thus requiring a less potent regulatory response to establish chronicity compared to systemic helminths. This suggests that the immunomodulatory demand is proportional to the pathogen’s invasiveness.

Furthermore, the significant inter-individual variation in the patient group (Range: 18.64 – 65.43 pg/mL) indicates that factors beyond mere infection status influence IL-10 production. This variability may be attributed to differences in parasite burden, genetic predisposition in host immune responses, or the presence of co-infections, as highlighted in studies on cytokine polymorphisms by (35). The fact that some infected individuals exhibited IL-10 levels near the control range suggests that the immunoregulatory phenotype is not universal and that some hosts may mount a less suppressed, and potentially more effective, immune response.

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