Prevalence, Spatial distribution, and Risk Factors of Enterobius vermicularis among Children in Kidapawan City, Philippines

doi:10.21203/rs.3.rs-4395132/v1

The high prevalence of Enterobius vermicularis is typically associated with sociodemographic characteristics and hygiene practices as risk factors. In this study, a geospatial tool was used to determine the distribution of Enterobius vermicularis across Kidapawan City, Philippines. A cohort of 138 respondents was included, and the prevalence of enterobiasis was determined using the scotch tape method, which is considered the gold standard for Enterobius vermicularis identification. An adopted survey tool was used to identify the associated risk factors and was analyzed using the Pearson product-moment correlation coefficient. A geospatial mapping tool was used to visualize the distribution of enterobiasis among children. The results showed a 15.21% prevalence of Enterobius vermicularis infection in the rural area of Kidapawan City, Philippines. The results also showed that age (p = 0.000), mother’s educational level(p = 0.009), handwashing after toileting (p = 0.001) and before eating (p = 0.006), bathing without assistance (p = 0.002), and sharing a bed (p = 0.001) were all significant risk factors that may contribute to the prevalence of enterobiasis. The study provides the need for comprehensive public health interventions targeting both individual hygiene practices and socioeconomic factors to effectively control and prevent the spread of E. vermicularis infection within the community.

Enterobius vermicularis

geospatial mapping

spatial distribution

Intestinal helminths are present in more than 3.5 billion people globally and is one of the most prevalent and undertreated public health issues in developing nations [1]. The cosmopolitan parasite Enterobius vermicularis affects more than 200 million individuals globally, with those living in tropical regions and having children in school being the most vulnerable. Pinworm infections are caused by the accidental ingesting infected pinworm eggs found on fingers, clothing, bedding, and other contaminated surfaces [2]. Although several neglected parasitic diseases have readily available tools for their control and elimination, public awareness and interventions are not evident.

One study revealed that in Guangdong, China, the prevalence of three species of soil-transmitted helminthiases (ascariasis, trichuriasis, and hookworm disease) has decreased owing to recent rapid economic development and improvements in hygiene; however, the prevalence of E. vermicularis infection remains high [3]. The prevalence of E. vermicularis infection in children in Gaozhou was 54.86%, which is relatively high. These are also observed in countries such as Venezuela (63%), Argentina (43%), Laos (35%), and Turkey (23%) [4]. A 2020 study in Southeast Asia revealed that the incidence of E. vermicularis infection varies between 0% and 50.90%. The most frequently affected group was schoolchildren who lived in crowded conditions and had inadequate personal hygiene [5]. In the Philippines, a study showed that 45 of 80 (56%) children from selected municipalities of Lucban, Quezon, were positive for intestinal parasitic infections. Trichuris trichiura (32.5%) had the highest prevalence among the recovered parasites, followed by Ascaris lumbricoides (26.25%), E. vermicularis (13.75%), and hookworm eggs (10%) [6].

Several risk factors of enterobiasis have been identified, particularly in preschool-aged children. These include poor personal hygiene practices, such as not washing hands with soap after using the toilet and before eating, and habits such as nail biting and finger sucking, which can increase the likelihood of ingesting eggs from contaminated surfaces. Family aggregation is another risk factor, as enterobiasis is more likely to spread within households in which children share beds or bedrooms. Furthermore, the living environment can play a role, with factors such as carpeted floors (difficult to clean), concrete floors (harboring eggs longer), playing on the floor (increased exposure), and living in non-apartment dwellings (potentially less control over hygiene) all contributing to a higher risk of infection. [3, 7].

Despite the availability of simple control and elimination methods for many neglected parasitic diseases, public awareness remains low and widespread interventions have not been implemented. This study adopted a unique approach by employing multivariate analysis to investigate how demographics, personal hygiene, and residential sanitary conditions affect pinworm infections among children. Additionally, spatial mapping was used to visualize the prevalence and spread of infections in Kidapawan City. By utilizing these methods, this study aimed to provide a deeper understanding of the factors influencing pinworm infections, with the hope of informing more effective public health interventions and raising awareness of Enterobius vermicularis infections.

Sociodemographic Profile and Prevalence of E. vermicularis among Children

Among the demographic profiles, only two factors were significantly associated with the prevalence of E. vermicularis. These factors were the age of the children (p = 0.000) and the mother’s educational level (p = 0.009). This suggests that behaviors commonly observed among children, such as playing outside, getting their hands dirty, going barefoot, and/or neglecting cleanliness, may encourage E. vermicularis infection. Notably, children between the ages of 3 and 6 years were found to be most susceptible to contracting E. vermicularis, which is consistent with findings from other studies.

Table 1

Association of Socio-demographic Profile and Prevalence Rate of *E. vermicularis* among Children in Kidapawan City, Philippines
Sex	Positive with E. vermicularis		df	p-value
Sex	Freq.	%	df	p-value
male	13	9.4	1	0.327
female	16	11.6	1	0.327
Age of Children			2	0.000
1 to 3 years old	4	2.9
4 to 6 years old	21	15.2
7 to 9 years old	4	2.9
Number of Family Members			1	0.236
5 and less than five	19	13.8
greater than five	10	7.2
With Older Brother/s or Sister/s			1	0.301
Yes	17	12.3
No	12	8.7
With Younger Brother/s or Sister/s			1	0.538
Yes	13	9.4
No	16	11.6
Father’s Education Level				0.358
Primary School	14	10.1	2
Secondary School	11	8.0
Bachelor’s degree or higher	4	2.9
Mother’s Education Level			2	0.009
Primary School	9	6.5
Secondary School	19	13.8
Bachelor’s degree or higher	1	0.7
Father’s Occupation			3	0.226
Agricultural	2	1.4
Trade/Business owner	0	0.0
Government/Private officer	1	0.7
Others	29	2.1
Mother’s Occupation			3	0.687
Agricultural	0	0.0
Trade/Business owner	1	0.7
Government/Private officer	0	0.0
Others	29	21.0
Father’s Income			4	0.580
< P 5,000	11	8.0
P 5,000 – P 9,999	15	10.9
P 10,000 –P14,999	3	2.2
P 15,000 – P19,000	0	0.0
> P 20,000	0	0.0
Mother’s Income			4	0.579
< P 5,000	24	17.4
P 5,000 – P 9,999	3	2.2
P 10,000 –P14,999	0	0.0
P 15,000 – P19,000	1	0.7
> P20,000	1	0.7

Personal Hygiene and Prevalence Rate of E. vermicularis among Children

Table 6 highlights significant personal hygiene practices associated with the prevalence of Enterobius vermicularis infection. Individuals who did not wash their hands before eating (p=0.001), neglected to wash their hands after using toilet facilities(p=0.006), did not have family assistance(p=0.002), and shared a bed with family members(p=0.001) were at a higher risk of infection. These findings suggest the importance of maintaining good personal hygiene habits to reduce the risk of Enterobius vermicularis infection. Regular handwashing, especially before eating and after using the toilet, as well as bathing with assistance when necessary and avoiding bed-sharing are crucial preventive measures to minimize the prevalence of this parasitic infection.

Table 2. Association of Personal Hygiene and Prevalence Rate of E. vermicularis among Children in Kidapawan City, Philippines

Personal Hygiene Possible Risk Factors	Positive with E. vermicularis		df	p-value
Personal Hygiene Possible Risk Factors	Freq.	%	df	p-value
Are children …
1. washing their hands before eating?			1	0.001
Yes	26	18.8
No	3	2.2
2. washing their hands after using toilet facilities?			1	0.006
Yes	27	19.6
No	2	1.4
3 keeping their fingernails short?			1	0.852
Yes	29	21.0
No	0	0.0
4. sucking their fingers?			1	0.174
Yes	9	6.5
No	20	14.5
5. playing with others?			1	1.00
Yes	28	20.3
No	1	0.7
6. taking a bath before sleeping?			1	0.646
Yes	24	17.4
No	5	3.6
7. taking a bath after waking up?			1	0.574
Yes	27	19.6
No	2	1.4
8. bathing without the assistance of family members?			1	0.002
Yes	18	13.0
No	11	8.0
9. washing their underwear without the help of family members?			1	0.348
Yes	3	2.2
No	26	18.8
10. sharing a towel with others?			1	0.506
Yes	19	13.8
No	10	7.2
11. sharing a bed with family members?			1	0.001
Yes	23	16.7
No	6	4.3
12. having been dewormed of parasites?			1	0.936
Yes	17	12.3
No	12	8.7
Household Sanitary Conditions Risk Factors
1. style of residence			1	0.355
single-family detached home	29	21.0
apartment	0	0.0
2. structure the house is made of			1	0.069
concrete	5	3.6
wood	24	17.4
3. type of bed children have			1	0.042
wood or spring mattress	20	14.5
floor mats	9	6.5
4. frequency the children beddings are changed			2	0.704
once a week	25	18.1
once every two weeks	2	1.4
once a month or more	2	1.4
5. cleaning their house everyday			1	1.00
Yes	29	21.0
No	0	0.0

Prevalence of E. vermicularis among Children in Kidapawan City, Philippines

The prevalence of E. vermicularis was based on a population size of 27,144 and a response distribution of 90 percent, with a margin of error of 5% and 95% confidence level. Figure 1A shows the geographical distribution of E. vermicularis in Kidapawan City, Philippines. The results indicated that 29 of the 138 respondents (15.21%) tested positive for E. vermicularis. Owing to the circumstances that support the infection, this reflects a rather high prevalence despite the rigorous deworming efforts of the local health office. Therefore, E. vermicularis remains a significant parasitic illness in Kidapawan.

Significance of the Association between Sociodemographic Profile and Prevalence Rate of E. vermicularis among Children in Kidapawan City, Philippines

Figure 1B-C shows the geographical distribution of significant sociodemographic factors. This showed that only two sociodemographic factors were significantly associated with the prevalence of E. vermicularis: the age of the children (p=0.000) and the mother’s educational level (p=0.009). This implies that behaviors among children, such as playing outside, getting their hands dirty, going barefoot, and/or completely ignoring cleanliness, as most children do, encourage E. vermicularis infection. Children aged 3–6 years were most likely to contract E. vermicularis, which is consistent with the results of other studies.

Considering the association of personal hygiene as a possible risk factor and the prevalence of E. vermicularis, Figure 1D-G shows the geographical distribution of significant risk factors: (D) washing their hands before eating (p=0.001), (E) washing their hands after using toilet facilities (p=0.006), (F) bathing without the assistance of family members (p=0.002), and (G) sharing a bed with family members (p=0.001). Additionally, only the type of childbed was significantly associated with the association between household sanitary condition risk factors and the prevalence of E. vermicularis.

The 15.21% prevalence rate of Enterobius vermicularis infection suggests a significant burden of this parasitic infection in different barangays of Kidapawan City, Philippines. According to a previous study [6], enterobiasis is a major public health concern in regions with socioeconomic disadvantages and insufficient hygiene practices. The prevalence rate among children is known to be affected by factors including age, mother's education level, handwashing practices, and bathing and bed-sharing habits, as reported in numerous studies. [10–14]. In this study, the association between the age of children and mothers’ education level was a significant determinant of enterobiasis. Several studies have reported that children are more prone to infection because of their limited self-awareness and inadequate self-management skills [3, 8]. Moreover, parental knowledge of enterobiasis reduces the risk of in children getting infected [3, 9]. Thus, strengthening handwashing and health habits at home can control the spread of Enterobius vermicularis infection. Additionally, we reported that maintaining poor hygiene might contribute to contracting Enterobius vermicularis. Insufficient hand hygiene increases the risk of ingesting Enterobius vermicularis eggs, which may be present in contaminated nails [12]. Bathing without assistance may result in incomplete cleaning, leaving pinworm eggs around the perianal area and thus increasing the risk of reinfection [12, 13]. Moreover, pinworm infection can spread via bed sharing owing to the transfer of eggs from infected persons onto bedding or night clothes [14, 15].

An important strength of this study is the use of a geospatial mapping technique to visualize the distribution of Enterobius vermicularis infection, allowing for targeted public health interventions and resource allocation in Kidapawan City, Philippines. Given the significantly higher rates of pinworm infection in Amas, Paco, Sudapin, and Ilomavis compared to the other 40 barangays in Kidapawan City, implementing educational programs, awareness campaigns, and preventive measures in these areas can effectively address the issue, reduce the prevalence of E. vermicularis, and aid in targeted intervention strategies and public health planning. The study also recognized limitations such as its sample size, which may not fully represent the entire population of Kidapawan City. Additionally, the use of the Scotch tape technique for data collection may have resulted in underestimation of the true prevalence of enterobiasis. Although this method is considered the gold standard for the identification of Enterobius vermicularis, it has also been reported to have lower sensitivity than other diagnostic methods. Despite these limitations, this study highlights the need for targeted public health interventions aimed at improving hygiene practices and raising awareness about enterobiasis, particularly in rural areas with poor socioeconomic conditions.

Research Respondents

This study included 138 young children with a response distribution of 90 percent, and the margin of error was set at 5%, with a 95 percent confidence level. Children in Kidapawan, Philippines under the age of ten who agreed to participate and whose parents or legal guardians consented were included.

Sample Collection

The local population was clustered by barangay and respondents were chosen randomly from within each barangay in Kidapawan. For sample collection, children who were not residents of Kidapawan City, who did not complete the three days of sampling, and who took a bath or had bowel movements before sample collection were excluded from the study. The Scotch tape technique was used to identify E. vermicularis among respondents. Briefly, perianal skin with a transparent tape was used to collect pinworm eggs around the anus. Before bowel movement and bathing, the samples were collected between 5:30 AM and 9:00 AM. The samples were collected using adhesive or Scotch tape (25.4 x 76.2 mm). Adhesive tape was pressed against the child's perianal region and attached to a glass slide. Cellulose tape was firmly pressed to remove trapped air bubbles. The presence of E. vermicularis ova was checked on the slides.

Identification of associated risk factors

An adapted survey questionnaire [5] was used to gather demographic, personal hygiene, and household sanitary data from the respondents. Briefly, parents or primary caregivers of children were asked to sign a consent form before sample collection and were asked to fill out a questionnaire about demographic data, potential risk factors involved, personal hygiene, and household sanitary conditions using a questionnaire through face-to-face interviews.

Geospatial Mapping

Coordinates were acquired for each collection site and, together with the mean score of each variable, spatial mapping was generated using QGIS Desktop 3.30.3 Hertogenbosch.

Statistical analysis

The Pearson product-moment correlation coefficient was used to identify the association between sociodemographic and risk factors and the prevalence of E. vermicularis infection.

This study highlights the significant prevalence of E. vermicularis infections among children in Kidapawan City, Philippines, and identifies important risk factors associated with the transmission of this parasitic infection. These findings underscore the need for comprehensive public health interventions targeting both individual hygiene practices and socioeconomic factors to effectively control and prevent the spread of E. vermicularis infection within the community.

Institutional Review Board Statement

The study was conducted in accordance with the Declaration of Helsinki and approved by the Institutional Review Board (or Ethics Committee) of The University of The Immaculate Conception Protocol Code GS-41-01-23 February 16, 2023.

Informed Consent Statement: Informed consent and assent were obtained from the parents'/guardians' agreement to have their child participate in the study.

Conflicts of Interest:

The authors declare no conflicts of interest.

Funding:

This research was funded by the University of Immaculate Conception Research and Innovation Center.

Author Contribution

Writing – original draft, Z.V.O, A.A.H.Jr. Investigation, Z.V.O.; Supervision, A.A.H.Jr; Writing – Review & editing, A.A.H.Jr. All authors have read and agreed to the published version of the manuscript.

Data Availability

All data generated or analyzed during this study are included in this published article.

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No competing interests reported.

Prevalence, Spatial distribution, and Risk Factors of Enterobius vermicularis among Children in Kidapawan City, Philippines

Status:

Version 1

Abstract

Figures

Introduction

Discussion

Methods