Enterobiasis among Yemeni children: a cross-sectional study

Abstract

Enterobiasis is a highly infectious parasitic disease spreading worldwide including Yemen. Therefore, this study aimed to investigate the prevalence and risk factors of enterobiasis among Yemeni children in Dhamar governorate. A total of 402 children (aged 1–12 years) participated in this cross-sectional survey carried out at Thamar University Al-Wahdah Teaching Hospital (TUWTH), between 2018 and 2019. Enterobius vermicularis infection was examined using the adhesive tape technique. Association between risk factors and enterobiasis were measured by prevalence ratio (PR). The overall prevalence of enterobiasis was found to be 29.4% (118/402). Risk factors that showed independent association with the infection were child’s care responsibility (PR = 1.90; 95% CI = 1.37–2.63; P = 0.001); irregular washing hands before meals (PR = 2.01; 95% CI = 1.32–3.05; P = 0.003); habit of nail biting or cutting by teeth (PR = 1.61; 95% CI = 1.18–2.21; P = 0.002); habit of putting toys or pen in mouth (PR = 1.58; 95% CI = 1.19–2.10; P = 0.002); frequent anal itching (PR = 1.46; 95% CI = 1.10–1.93; P = 0.016); using anthelmintic during the last six months (PR = 1.68; 95% CI = 1.20–2.36; P = 0.011); and parents have no knowledge on preventive measures (PR = 1.62; 95% CI = 1.04–2.53; P = 0.036). Prevalence of enterobiasis among Yemeni children in Dhamar governorate is high with higher infection rate among those aged 1–6 years. Health education and mass treatment are highly recommended among this poor population.

Introduction

Enterobiasis, known as pinworm infection, is a highly contagious parasitic disease that is found all over the world. A human intestinal helminth named Enterobius vermicularis (pinworm or threadworm) causes it (Burkhart and Burkhart 2005). The most common mode of infection with E. vermicularis is a faecal-oral route, retroinfection also occurs (Cook 1994). This parasite's infective form is embryonated eggs that can survive for several weeks and can be transmitted from one person to another or to one's self by direct or indirect contact with contaminated hands, bedding, habitation objects, foods, drink, animal hair, dust, and other vehicles (Kim et al. 2013; Park et al. 2005). Enterobiasis can affect all age groups, with children being more commonly infected than adults (Nithikathkul et al. 2001). Many risk factors have been linked to the incidence of this infection among children who have more interaction with one another and are frequently exposed to overcrowding and inadequate hygiene (Lohiya et al. 2000).

Medical scientists and health providers commonly describe enterobiasis as a mild parasitic infection characterized by nocturnal anal pruritus (Burkhart and Burkhart 2005). However, such a clinical feature affects victims’ well-being; disturbs their sleep and causes nervous disorders (Kang et al. 2006). It is due to the fact that the gravid worm travels at night from the rectum through the anal canal to lay eggs on the perianal area (Tandan et al. 2002). The medical importance of E. vermicularis comes from being widespread, highly infectious, and difficult to eliminate (Olivares et al. 2002). This annoying worm, measured about one centimeter, may continue to reinfect susceptible persons throughout their life. Other clinical symptoms of the disease include irritation and scratching the anal area due to an allergic reaction to the deposited eggs, abdominal discomfort, loss of appetite and weight, and developmental retardation (Afrakhteh et al. 2016; Tsibouris et al. 2005; Wang et al. 2016). Although many studies reported serious consequences of enterobiasis among children, those are mostly inflammatory reactions to the worms penetrating the large intestine or appendix wall or migrating into the female genital organs and the abdominal cavity (Sah and Bhadani 2006).

Unlike other intestinal parasites, E. vermicularis eggs are infrequently seen in the stool specimen. It is only about 5% of the cases estimated to show positive results when the stool is the used specimens for detecting the parasite eggs (Chu et al. 2012). Hence, the diagnosis of this parasite mainly depends on finding eggs of the parasite in the area around the anus using swabs or adhesive tape techniques.

In Yemen, there are no published reports indicating the prevalence and risk factors of enterobiasis among children. What are available are studies that used stool as a sample to examine intestinal parasites (Al-Mekhlafi et al. 2016; Alyousefi et al. 2011). As mentioned above, stool examination is not recommended for diagnosing pinworm infection. Within this context, this cross-sectional study was aimed to investigate the prevalence and risk factors of E. vermicularis infection among children treated at TUWTH in Dhamar governorate, Yemen.

Methods

Study area

Dhamar governorate (15°40′N 43°56′E) is located at the central area of the western highland’s region of Yemen, 1600–3200 m above sea level. There are only two general public hospitals in this area, TUWTH and Dhamar General Hospital. The study was held at TUWTH, which is located in Ma'bar city, the second urban collection of the Dhamar governorate, at a height of 70 km and 2331 m above sea level. Ma'bar is a city in Jahran District that has a population of roughly 130,975 people and occupies an area of 558 km². It has annual averages temperature and rainfall of about 16 °C and 377 mm, respectively. The agriculture is the principle economic activity of the population.

Study design

This survey was conducted between May 2018 and June 2019. It was a cross-sectional hospital-based survey among children visiting TUWTH’s outpatient clinics with their parents. Children aged 1–12 years were randomly enrolled using a simple systematic sampling method. In this study, more than one child from the same family was excluded. The adhesive tape technique using the cellophane tape (cellulose tape) was used for investigating the prevalence of E. vermicularis infection. The specimens were collected from the perianal surface of children using a piece of clear cellophane tape. The samples were mounted on a glass slide and examined using the light microscope (10 × and 40 × magnifications) in the Medical Laboratory Department, TUWTH. A pretested structured questionnaire was designed to collect sociodemographic characteristics and hygiene behaviours information which seem to be potential risk factors for enterobiasis. Children’s parents were interviewed face-to-face by trained medical students.

Sample size and study population

The sample size needed for this investigation was estimated using a 95 percent confidence level and a precision of 0.05 as the desired precision. Because no data from the Dhamar governorate is available, a 50% E. vermicularis infection was expected. A total of 384 children were determined to be the minimum sample size required. To account for the non-response rate, the sample size was increased by 10%, resulting in a sample size of 422. Of this planned sample size, only 402 children were included in the final analysis; voluntarily examined and their parents completed the questionnaire.

The protocol of this study was approved by the Thamar University Medical Ethics Committee (TUMRC) of Thamar University Faculty of Medicine and Health Sciences (TUFMHS), Dhamar (Reference Number: TUMRC-18001). All examinations were carried out with permission from the children’s parents. Oral informed consent was obtained before commencing the survey.

Statistical analysis

The SPSS version 25 application was used to analyze the data. The Chi-square test was performed to analyze the differences in the prevalence of enterobiasis between the risk factor groups using a univariate analysis. Risk factor’s category with higher prevalence of enterobiasis was coded as 1, another category was coded as 0 (reference group). Variables that showed a difference with a P-value ≤ 0.20 were used to develop a multiple analysis. Prevalence ratios (PR) for risk factors analysis were calculated by Poisson model incorporating the robust sandwich variance (RSV) as well as using the bootstrap technique. P-value * 0.05 was considered as significant.

Results

Distribution of potential risk factors

A total of 402 children (aged 1–12 years) participated in this survey and examined for E. vermicularis infection using the adhesive tape technique. Majority (71.1%–89.1%) of the children were 1–6 years, their mothers had less than secondary education, belonged to families living under the poverty line (≤ 150 USD/month), had less than three times showers per week, irregularly wash their hands with soap after defecation and their parents had no knowledge on the preventive measures against enterobiasis. Potential risk factors such as gender male, rural residency, family size of ≥ 5 members, and irregular washing hands before meals as well as vegetables or fruits were distributed among almost half (43.8%–58.5%) of the study subjects. Other potential risk factors showed lower distribution values ranging from 9.7% to 37.6%. General distribution of the potential risk factors of enterobiasis among the children is shown in Table 1.

Table 1.

General distribution of potential risk factors of enterobiasis among Yemeni children in Dhamar Governorate (n = 402)

Potential risk factors	Frequency n (%)
Sociodemographic characteristics
Age (1–6 years)	319 (79.4)
Gender (boy)	219 (54.5)
Residency (rural)	235 (58.5)
Father’s education level (< secondary education)	93 (23.1)
Mother’s educational level (< secondary education)	288 (71.6)
Household income (≤ 150 USD/month)	335 (83.3)
Family size (≥ 5 members)	217 (54.0)
Source of drinking water (untreated)	139 (34.6)
Child’s care responsibility (other than mother)	39 (9.7)
Visiting or living in crowded conditions such as kindergartens, schools, refugee camps (yes)	153 (38.1)
Hygiene behaviors
Frequency of bathing per week (< 3 times)	358 (89.1)
Regular washing hands before meals (no)	223 (55.5)
Regular washing hands with soap after defecation (no)	326 (81.1)
Regular washing vegetables or fruits before eating (no)	176 (43.8)
Habit of nail biting or cutting by teeth (yes)	145 (36.1)
Habit of fingers licking or sucking (yes)	74 (18.4)
Habit of putting toys or pen in mouth (yes)	55 (13.7)
Accumulation of dirt beneath nails (yes)	151 (37.6)
Frequent anal itching (yes)	70 (17.4)
Using anthelmintics during the last six months (yes)	43 (10.7)
Parents knowledge of preventive measures (no)	286 (71.1)
Ability of children or parents to recognize the picture of the pinworm (yes)	82 (20.4)

General prevalence of enterobiasis

General prevalence of enterobiasis was found to be 29.4% (118/402) among children in Jahran district, Dhamar Governorate, Yemen (Fig. 1).

Fig. 1.

Prevalence of Enterobius vermicularis infection among Yemeni children in Dhamar governorate

Risk factors of enterobiasis

Univariate analysis showed no significant difference (P * 0.05) in the prevalence of enterobiasis with gender, residency, parent’s educational level, household income, source of drinking water and habit of fingers licking or sucking. In contrast, there was significant difference (P * 0.05) in the prevalence of enterobiasis with the listed sociodemographic and hygiene behaviors illustrated in Table 2.

Table 2.

Associations of potential risk factors with Enterobius vermicularis infection among Yemeni children in Dhamar Governorate (n = 402)

Variable	Univariate analysis		Multivariate analysis
	Enterobiasis n (%)	P value	PR (95% CI)	P value
Age (years)
1–6	101 (85.6)	0.046	1.38 (0.91–2.09)	0.134
7–12	17 (14.4)		1
Gender
Boy	70 (59.3)	0.209
Girl	48 (40.7)
Residency
Rural	69 (58.5)	0.996
Urban	49 (41.5)
Father’s educational level
< Secondary education	26 (22.0)	0.736
≥ Secondary education	92 (78.0)
Mother’s educational level
< Secondary education	91 (77.1)	0.116	0.78 (0.55–1.09)	0.137
≥ Secondary education	27 (22.9)		1
Household income (USD/month)
≤ 150	103 (87.3)	0.170	1.07 (0.71–1.61)	0.773
> 150	15 (12.7)		1
Family size (members)
≥ 5	80 (67.8)	< 0.001	1.25 (0.88–1.79)	0.243
< 5	38 (32.2)		1
Source of drinking water
Untreated sources	48 (40.7)	0.097	0.92 (0.70–1.21)	0.589
Treated sources	70 (59.3)		1
Child’s care responsibility
Other than mother	23 (19.5)	< 0.001	1.90 (1.37–2.63)	0.001
Mother	95 (80.5)		1
Visiting or living in crowded conditions
Yes	65 (55.1)	< 0.001	1.13 (0.81–1.57)	0.503
No	53 (44.9)		1
Frequency of bathing per week
< 3 times	112 (94.9)	0.015	1.77 (0.93–3.38)	0.079
≥ 3 times	6 (5.1)		1
Regular washing hands before meals
No	94 (79.7)	< 0.001	2.01 (1.32–3.05)	0.003
Yes	24 (20.3)		1
Regular washing hands with soap after defecation
No	107 (90.7)	0.002	1.53 (0.97–2.42)	0.073
Yes	11 (9.3)		1
Regular washing vegetables or fruits before eating
No	64 (54.2)	0.006	0.97 (0.74–1.28)	0.826
Yes	54 (45.8)		1
Habit of nail biting or cutting by teeth
Yes	66 (55.9)	< 0.001	1.61 (1.18–2.21)	0.002
No	52 (44.1)		1
Habit of fingers licking or sucking
Yes	28 (23.7)	0.076	1.23 (0.83–1.82)	0.309
No	90 (76.3)
Habit of putting toys or pen in mouth
Yes	26 (22.0)	0.002	1.58 (1.19–2.10)	0.002
No	92 (78.0)		1
Accumulation of dirt beneath nails
Yes	58 (49.2)	0.002	0.99 (0.73–1.34)	0.949
No	60 (50.8)		1
Frequent anal itching
Yes	42 (35.6)	< 0.001	1.46 (1.10–1.93)	0.016
No	76 (64.4)		1
Using anthelmintic during the last six months
Yes	24 (20.3)	< 0.001	1.68 (1.19–2.36)	0.011
No	94 (79.7)		1
Parents knowledge on preventive measures
No	101 (85.6)	< 0.001	1.62 (1.04–2.53)	0.036
Yes	17 (14.4)		1
Ability of children or parents to recognize the picture of the pinworm
Yes	34 (28.8)	0.007	0.79 (0.57–1.10)	0.188
No	84 (71.2)		1

Multivariate analysis just confirmed the following variables as a real independent risk factors for E. vermicularis infection among the children in Dhamar Governorate: Child’s care responsibility (PR = 1.90; 95% CI = 1.37–2.63; P = 0.001); irregular washing hands before meals (PR = 2.01; 95% CI = 1.32–3.05; P = 0.003); habit of nail biting or cutting by teeth (PR = 1.61; 95% CI = 1.18–2.21; P = 0.002); habit of putting toys or pen in mouth (PR = 1.58; 95% CI = 1.19–2.10; P = 0.002); frequent anal itching (PR = 1.46; 95% CI = 1.10–1.93; P = 0.016); Using anthelmintic during the last six months (PR = 1.68; 95% CI = 1.20–2.36; P = 0.011); and parents have no knowledge on preventive measures (PR = 1.62; 95% CI = 1.04–2.53; P = 0.036). However, this doesn’t negate the risk probability of other variables may be in case studied on other study population or study area.

Discussion

To the best of our knowledge, this is the first survey to assess the prevalence of E. vermicularis infection in Yemen using an appropriate test, the cellophane tape technique. The present study revealed a relatively high prevalence (29.4%) of enterobiasis among Yemeni children aged 1–12 years. This finding is in agreement with some previous studies conducted on preschool and primary school children in some regions of different countries around the world over the past ten years. However, there are some other studies that have not reported a high incidence of enterobiasis among children.

The prevalence of enterobiasis reported by the present study was comparable to those reported in Jordan (55.2%), Southern China (54.9%), Myanmar (47.2%), Romania (42.8%), Seri Lanka (38.0%), and the Philippines (36.3%) (Bustami and Khraisha 2010; Chai et al. 2015; Gunawardena et al. 2013; Li et al. 2015; Neghina et al. 2011; Totanes et al. 2009). However, it was considerably higher than those reported in Taiwan (0.62%), Iran (7.1%), Korea (10.5%), Malaysia (12.5%), Egypt (15.2%), and Mexico (18.3%) (Afrakhteh et al. 2016; Anuar et al. 2016; Bayoumy et al. 2016; Chang et al. 2009; de la Luz Galván-Ramírez et al. 2019; Lee et al. 2011).

The prevalence of enterobiasis in this study was not a pure coincidence. The present study confirmed that the exposure to infected subjects and hygiene behaviours had a significant and independent association with this prevalence. The strength of this association was statistically well measured. Multivariate analysis indicated that enterobiasis was associated with washing hands before meals. Children who did not practice such hygienic behaviours had a higher prevalence risk of acquiring the infection. This was similar to findings in previous reports (Gyawali et al. 2010; Li et al. 2015; Suraweera et al. 2015). Other interesting results of the present study is the significant association between E. vermicularis infection and certain habits, such as nail-biting using teeth to tear and open packages, and putting toys or pen in the mouth. Such unhygienic behaviours have been reported as independent risk factors for enterobiasis among preschool and primary school children in China (Bustami and Khraisha 2010). E. vermicularis has a very simple transmission cycle, only from two to four weeks in order to mature the eggs to adult worms. Hence, the contamination of toys and school equipment with E. vermicularis can be easily occur (Li et al. 2015). This study also showed a significant association between enterobiasis and parental knowledge on preventive measures. This result is in consistent with a previous study concluding that parental knowledge might be one of the most important risk factors for enterobiasis in children (Kim et al. 2010). The current study also indicated that children cared for by their parents have a higher prevalence of enterobiasis and this was in agreement with an earlier study carried out in China (Wang et al. 2016). This can be interpreted as an effect of the low educational level among children’s mothers who participated in this study. Perianal itching was revealed by this study to be a highly significant risk factor for E. vermicularis infection. It is well known that such clinical symptom is one of the most predictors of enterobiasis (Li et al. 2015; Totanes et al. 2009). In the present study, the anthelmintic during the last six months was significantly associated with the prevalence of enterobiasis. A similar finding has been reported in previous studies (Anuar et al. 2016; Chai et al. 2015). Two probabilities could be explain this case, one is that the anthelmintic doesn’t kill all larvae and mature forms of E. vermicularis or there’s only one dose used without repeat (Hong et al. 1979; Kim et al. 2010). Second, this could be ascribed to poor hygiene promotion that affects the risk of reinfection (Gungoren et al. 2007).

Conclusion

Based on the results of this study, the prevalence of enterobiasis among Yemeni children in Dhamar governorate is high. E. vermicularis is found to be higher among those aged 1–6 years. The risk factors associated significantly with the infection are child’s care responsibility, irregular washing of hands before meals, certain bad habits such as nail biting using the teeth for tearing things, putting toys or pen in the mouth, frequent anal itching, using anthelmintic during the last six months, and parents having no knowledge on preventive measures. Mass treatment along with effective educational programs should be performed in this area in order to control infection. However, more survey studies in different parts of Dhamar governorate are important for reaching a real epidemiological picture.

Author contribution

AHA was involved in all phases of the study, including study design, data collection, data analysis and interpretation, the write-up of the manuscript, statistical analysis of data and the critical revision of the manuscript for publication; YAA, MAA and AH Amer were involved in the study design, specimen examination and revision of the manuscript; and MMA, FHA, RHA, ESA, SAA, TMA were involved in the collection of the data, specimen examination and write-up of the first draft of the manuscript. All authors read and approved the final manuscript.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Availability of data and materials

Data supporting the conclusions of this article are included within the article. The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

Declarations

Conflict of interests

The authors declare that they have no competing interests.

Ethics approval and consent to participate

The protocol of this study was approved by the Thamar University Medical Ethics Committee (TUMRC) of Thamar University Faculty of Medicine and Health Sciences (TUFMHS), Dhamar (Reference Number: TUMRC-18001). All examinations were carried out with permission from the children’s parents. Oral informed consent was obtained before commencing the survey.