Intestinal parasitic infection among rural schoolchildren in Taiz, Yemen: School-based assessment of the prevalence and associated risk factors

T. Alharazi

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Helminthologia

Zeitschriftendaten

Format: Zeitschrift
eISSN: 1336-9083
Erstveröffentlichung: 22 Apr 2006
Erscheinungsweise: 4 Hefte pro Jahr
Sprachen: Englisch

Intestinal parasite infections (IPIs) are a major source of high morbidity and mortality in low-income countries, with millions of people infected with parasitic infections (Pradhan et al., 2014; Sitotaw et al., 2020). Infections are often a severe health issue in many developing countries, such as Yemen (Efstratiou et al., 2017). These countries have infection rates of 30 – 60 %, compared to 2 % in developed countries (Kumar et al., 2019).

IPIs are a major public health concern on a global level, affecting primarily children in developing countries (Harhay et al., 2010)^. G. lamblia is one of the most prevalent causes of diarrhea globally, accounting for approximately 200 million cases each year and posing the risk of zoonotic transmission (Yaoyu et al., 2011). In contrast, E. histolytica is one of the most serious intestinal protozoa in terms of morbidity and mortality. It affects approximately 500 million people annually and causes amoebic dysentery and invasive amoebiasis in about 50 million people. It has killed about 100,000 people (Baxt et al., 2008). Also, infections by parasitic worms, mainly Schistosoma and soil-transmitted Helminthes, remain global burdens in low-income countries (Hotez et al., 2014; Mascarini-Serra, 2011).

The persistence of intestinal parasite infections in children has been linked to a variety of environmental and socioeconomic factors. (Bugssa, 2015; Dejenie et al., 2010; Mascarini-Serra, 2011). In Yemen, the prevalence of intestinal parasite diseases varies from region to region based on personal and societal hygienic, sanitation, and environmental conditions. (Raja’a et al., 2001).

In a few Yemeni provinces, some school-based studies have been carried out, including Taiz (Al-Harazi, 2016; T. Alharazi et al., 2020), Sana’a (bin Mohanna et al., 2014), Aden (Al-Abd et al., 2021), Ibb (Alsubaie et al., 2016), Hadhramout (Al-Haddad et al., 2010), and Al-Mahweet (Alwabr et al., 2016). In one of the earliest large-scale studies on IPIs in Yemen, over 37,000 stool samples were examined from 1980 to 1982, leading to a prevalence rate of 53.0 % (Farag, 1985). A recent study in the urban region of Taiz revealed that 107 (27.8 %) of the 385 children examined for enteric parasites were positive (Alharazi et al., 2020). The majority of studies conducted in Taiz took place in urban areas. Many epidemiological studies have been carried out in Yemen, including Taiz, to investigate the prevalence of IPIs (Al-Harazi, 2016; T. Alharazi et al., 2020), with only a few studies focusing on the prevalence and distribution of Giardia (Al-Mekhlafi, H.M. et al. 2017) and Schistosoma infections (Alharazi et al.,2021). In addition, Taiz has many valleys and streams that provide water for drinking and domestic purposes and are considered major routes for Giardia transmission (Hisham et al., 2017). Furthermore, the snail vector of schistosomiasis is heavily prevalent in these streams and valleys, creating an environment that facilitates Schistosomiasis transmission (Sady H. et al., 2013). Thus, the current study aimed to determine the prevalence of intestinal parasites and risk factors among schoolchildren in rural communities in Taiz, southwestern Yemen.

Materials and Methods

Study design and study area

A cross-sectional survey was performed among schoolchildren in rural areas of the western Taiz governorate from 1 February to 31 March 2019. For this study, two rural districts (Almawasit & Sabir Almawadim) were recruited (Fig. 1). Convenience sampling was used to identify rural communities for this study. This was due to a security concern, as most of the districts in this governorate have been under siege since 2015. An official list provided by the Taiz Governorate’s General Directorate of Education was then used to select two schools from each district randomly. There are two schools selected, Khalid bin Alwaleed School in the Dhabab area and Saba School in the Aleayn area, both in Sabir Almawadim District. Furthermore, Dhabab Bani Hammad School and 26th September School have been selected from the Almawasit district. The schools were picked based on these criteria: there are over 100 students enrolled; the principal has agreed to be part of the study, and there haven’t been any threats of war or kidnapping.

A geographic map showing the study area (Almawasit & Sabir Almawadim) in Taiz governorate. The map was created by authors using the Esri ArcGIS 10.7 software

Taiz governorate (44.01°E and 13.34°N) is located in Yemen’s southern region, 280 kilometers from the capital Sana’a. It is surrounded on the west by the Red Sea, on the north by the governorates of Hodeida and Ibb, on the south by the governorate of Lahj, and on the east by the governorate of Al-Dhale. It is one of the country’s most densely inhabited governorates, with approximately 2.9 million aggregate population and 12,605 km² land area. Taiz governorate’s people are primarily farmers and merchants. Rural regions of Taiz governorates are dominantly inhabited by nearly 80 % of the population as compared to urban areas (20 %).

Taiz governorate consists of two biological zones: a mountainous highland zone on the east coast and a lowland coastal area on the west coast. The temperature fluctuates between relatively hot and cool during the year, with an average annual temperature of around 26 °C. The humidity level varies between 70 % and 90 %, and the average annual rainfall is about 200 mm. These areas are considered rural, with farmlands that depend on streams, underground wells, and ponds as the primary water source. The schools included in this study are close to valleys with streams, wells, and ponds. Most of the population in these areas worked in agriculture, and almost all mothers did not have a job, while fathers worked as farmers or laborers. Most houses do not have piped water, while only 20 % have electricity (connected to generators only at night).

Study population

Students in four (4) selected schools in rural areas of the Taiz governorate were included in the study. The participants were recruited through convenience sampling. Students attending grades 1 – 9 of formal education who participated in the study were invited to participate when we visited each school.

Of the 520 children eligible for the study, 15 refused to participate, did not provide their parents or guardians with an informed consent form, and 27 did not provide fecal and urine samples. As a result, a total of 478 schoolchildren aged 6 – 15 years old who provided suitable fecal or urine samples for analysis, filled out the questionnaires, and consented to participate in the study, were included in the analysis. Of the 478 students recruited, 118 were from the Khalid bin Alwaleed School, 123 from the Saba School in the Sabir Almawadim district, 112 from the Dhabab Bani Hammad School, and 125 from the 26^th September School in the Almawasit district. Most of the children had dirty unclipped fingernails and played outside with bare feet during the visit to the study areas. Some children spend part of their leisure time playing and swimming in streams or pools. In these study areas, poverty is prevalent, and poor housing and living conditions are typical.

Data and stool sample collection

Participants were lucidly informed of the purpose of the study prior to data collection. Parasites were detected by collecting 10 grams of fresh stool samples in screw-capped plastic containers of 100 mg capacity equipped with an applicator stick. The participants were instructed to collect sufficient samples aseptically. Following appropriate safety precautions and standard operating procedures, samples were immediately labeled and transported to the laboratory at ambient temperature. Using a wet mount preparation technique with saline, all stool samples were processed and examined for intestinal parasite cysts, trophozoites, eggs, and larvae using Olympus microscope model CX21 at 100x and 400x magnifications.

A face-to-face interview using a pretested and validated questionnaire was used to solicit information about the sociodemographic (age, gender, family size, and education level of parents) and environmental and behavioral factors (handwashing habits before meals, defecation habits, eating unwashed fruits and vegetables, source of drinking water, the pattern of swimming in a river/pond, washing clothes/utensils in open water, and the presence of animals in the house) (Al-Harazi, 2016).

Stool examination for parasites

Immediately after collection, saline or iodine wet preparations of stool samples were prepared and microscopically inspected using 10X and 40X objectives. Furthermore, stool sediments were examined using a formol-ether sedimentation method, following standard guidelines (Williams, 2000).

Analytical Statistics

The data was analyzed using the IBM SPSS Statistics version 20.0 (IBM Corp., Armonk, NY, USA). The odds ratio, the 95 % confidence interval, and the P value were calculated accordingly. A descriptive analysis of the distribution of the study subjects about the variables was performed. A fitted binary logistic regression analy sis model was completed after cross-tabulating each explanatory variable with the outcome variable while checking the fulfillment of chi-square assumptions. Univariate analysis was conducted to select variables for multivariate analysis. Finally, bivariate analysis was performed to choose variables for the multivariate analysis. All variables with a P value < 0.25 were used for the multivariate analysis utilizing forward stepwise logistic regression and were considered to have a significant association at P ≤ 0.05.

Ethical Approval and Informed Consent

Human participants were involved in all studies under the institution’s ethical committee’s ethical standards and the Helsinki Declaration of 1964 and its later amendments.

Results

The sociodemographic features of the participants in the study

A total of 478 students from four (4) primary schools in Almawasit and Sabir Almawadim districts participated in the study. The participants’ ages ranged from 6 to 15 years and were divided into two age groups according to a previous study (Mahdy et al., 2008) (i.e., 6 – 10 and 11 – 15). The 6 to 10-year-old age group accounted for 72.0 % (344/478) of participation, followed by the 11 to 15-year-old age group, which accounted for 28.0 % (134/478) (Table 1). Males made up more than half of the participants, 56.7 % (271/271). About 47.1 % (225) of the student’s parents are literate. Additionally, half of the participants (242/478) were from families with five or more members (Table 1).

Table 1

Socio-demographic characteristics of school children in rural communities of Taiz, Yemen.

Socio-demographic variables	categories	Frequency (n)	Percentage (%)
Age	≤10	344	72
	>10	134	28
Sex	Male	271	56.7
	Female	207	43.3
Parent’s educational status	literate	225	47.1
	illiterate	253	52.9
Family size	<5	236	49.4
	≥ 5	242	50.6
Washing hand before meals	Always	148	31.0
	sometimes	330	69.0
Defecation habits	Latrine	153	32.0
	Open field	325	68.0
Eating washed fruits and vegetables	Always	132	27.6
	sometimes	346	72.4
Source of drinking water	Protected tap water	147	30.8
	Unprotected stream/well	331	60.2
Swimming practice in rivers/ ponds	Sometimes	240	50.20
	Always	238	49.8
Washing clothes/utensil in open water sources	Sometimes	261	54.6
	Always	217	45.4
Dirty unclipping Fingernails	Always	144	30.1
	Sometimes	334	69.9
Existing of animals inside the house	No	258	54.0
	Yes	220	46.0

Prevalence of IPIs among study participants

As presented in Table 2, the total prevalence of parasitic intestinal infections among 478 examined rural schoolchildren in Taiz was 51.26 % (245/478). Notably, infections of protozoal parasites were predominantly observed over helminthic infections, accounting for 30.3 % (145/478) and 20.9 % (100/478) of all infections, respectively. G. lamblia and E. histolytica/dispar moshkovskii were the most common IPIs among schoolchildren (15.5 % (74/478) and 14.9 % (71/478), respectively). However, S. mansoni was the most common, 13.0 % (62/478) helminth, followed by Ascaris lumbricoides 3.8 % (18/478) and Trichurius trichuria 2.9 % (14/478). On the other hand, E. vermicularis was the least common helminth among schoolchildren, 1.3 % (6/478). Most of the students, 37.4 % (179/478), were infected with a single parasite species. In contrast, 4.4 % (21/478) and 1.7 % (8/478) of cases had double and triple infections.

Table 2

Prevalence of intestinal parasitic infections among schoolchildren in rural communities of Taiz, Yemen (2019 – 2020).

Parasite species	Number positive	Percentage (%)
Overall	245	51.26
Protozoa
Giardia lamblia	74	15.5
E.histolytica/dispar/moshkovskii	71	14.9
Total	145	30.3
Helminths
Schistosoma mansoni	62	13.0
Ascaris lumbercoid	18	3.8
Trichuris trichiura	14	2.9
Enterobius vermicularis	6	1.3
Total	100	20.9
Single	179	37.4
Double	21	4.4
Triple	8	1.7

Distribution of parasitic intestinal infections by gender among male and female participants

Table 3 reveals no statistically significant variation in overall protozoa infection rates based on gender. Both males and females were infected with G. lamblia at comparable rates (16.2 % vs. 14.5 %, respectively), with no statistically significant differences (P =0.602). In contrast, the overall helminthic infections prevalence rate was slightly higher among females (22.7 %) than males (19.6 %) without statistically significant differences (P =0.462).

Table 3

Distribution of intestinal parasitic infections among schoolchildren in rural communities of Taiz, Yemen (2019 – 2020) according to gender.

Parasite species	Gender^a Male n (%)	Female n (%)	P value
Protozoa
Giardia lamblia	44 (16.2)	30 (14.5)	0.602
E.histolytica/dispar/moshkovskii	41 (15.1)	30 (14.5)	0.846
Total	85 (31.4)	60 (29.0)	0.786
Helminths
Schistosoma mansoni	33 (12.2)	29 (14.0)	0.715
Ascaris lumbricoides	11 (4.1)	7 (3.4)	0.700
Trichuris trichiura	6 (2.2)	8 (3.9)	0.289
Enterobius vermicularis	3 (1.1)	3 (1.4)	0.739
Total	53 (19.6)	47 (22.7)	0.462

The total number examined was 271 for males and 207 for females.

The distribution of parasitic intestinal infections by age (IPIs among various age groups)

Table 4 shows statistically significant differences (P < 0.018) between the overall infection rates with protozoa by age group. Schoolchildren aged ≤10 years old, on the other hand, had a significantly higher (P< 0.014) infection rate with G. lamblia than those aged >10 years old (18.0 vs. 9.0 %, respectively). Though a higher infection rate of S. mansoni was observed among those aged > 10 years old than those aged ≤10 years old (15.7 % vs. 11.9 %, respectively), a significant difference (P > 0.05) was not found. In addition, Ascaris lumbricoides show a trend of infection rate among those aged ≤10 years old than those aged >10 years old (4.9 % vs. 0.8 %, respectively) with a statistically significant difference (P< =0.032).

Table 4

Distribution of intestinal parasitic infections among schoolchildren in rural communities of Taiz, Yemen (2019 – 2020) according to age.

Parasite species	Age group (years)^a		P value
	≤10 n (%)	>10 n (%)
Protozoa
Giardia lamblia	62 (18.0)	12 (9.0)	0.014
E.histolytica/dispar/moshkovskii	58 (16.9)	13 (9.7)	0.061
Total	120 (34.9)	25 (18.7)	0.018
Helminths
Schistosoma mansoni	41(11.9)	21(15.7)	0.273
Ascaris lumbricoides	17 (4.9)	1 (0.8)	0.032^b
Trichuris trichiura	10 (2.9)	4 (3.0)	1.000^b
Enterobius vermicularis	5 (1.4)	1 (0.8)	1.000^b
Total	73(21.2)	27(20.2)	0.386

The total number examined was 344 for age group ≤10 years and 134 for age group >10 years.

Calculated for Fisher’s exact test.

Risk factors associated with the prevalence of IPIs

Univariate analysis revealed seven factors associated with intestinal parasite infections (Table 5), including students aged ≤10 (OR= 1.391, 95% CI 1.054–1.837), students who do not practice unwashed hands before eating (OR= 1.753, 95% CI 1.157–2.657), defecate in open field (OR= 2.558, 95% CI 1.157–2.657), eating unwashed fruits and vegetables (OR= 3.299, 95% CI 2.252–4.831), drinking unprotected stream/well water (OR=2.457, 95% CI 1.689–3.575), dirty unclipping fingernail (OR= 2.725, 95% CI 1.868–3.976), and existing of animals inside the house (OR= 2.395, 95% CI 1.636–3.507). All other factors, including gender, family size, parents’ education level, swimming in streams, rivers, and ponds, and the use of open water sources in washing clothes and utensils, were not significantly linked to the prevalence of IPIs among schoolchildren. Multivariate analysis using forward stepwise logistic regression confirmed that schoolchildren with unwashed hands were 2.07 times more probably to present IPIs than those with clean hands before (Adjusted OR= 2.077, 95% CI 1.281–3.368), and those who defecated in the open field were twice as likely to get infected with IPs (Adjusted OR=1.869, 95% CI 1.216–2.874). In contrast, schoolchildren who ate washed fruits and vegetables were 0.289 less likely to exhibit IPIs than those who ate unwashed fruits and vegetables, and those who clipped their fingernails (Adjusted OR=0.545, 95% CI 0.352–0.845) were half as likely to exhibit IPIs compared with those with dirty unclipping (Table 5).

Table 5

Univariate and multivariate analysis of potential risk factors associated with intestinal parasitic infections among schoolchildren in rural communities of Taiz, Yemen

Variables		Infected %	OR (95% CL)	P value	AOR (95% CL)	P value
Age	>10	31.3	1		1
	≤10	43.6	1.391 (1.054-1.837)	0.014*	0.903(0.210-1.524)	0.601
Gender	Male	39.1	1
	Female	41.5	1.106(0.765-1.600)	0.591
Parent’s educational status	educated	41.3	1
	Non educated	39.1	0.912(0.633-1.316)	0.624
Family size	>5	41.2	1
	≤ 5	39.0	1.102(0.764-1.589)	0.602
Washing hand before meals	Always	31.0	1		1
	sometimes	44.0	1.753(1.157-2.657)	0.008*	2.07(1.281-3.368)	0.013*
Defecation habits	Latrine	32.0	1		1
	Open field	54.7	2.558(1.741-3.757)	0.001*	1.869(1.216-2.874)	0.004*
Eating washed fruits and vegetables	Always	27.5	1		1
	sometimes	55.6	3.299(2.252-4.831)	0.001*	0.289(0.010-1.37)	0.011*
Source of drinking water	Protected tap water	30.7	1		1
	Unprotected stream/well	52.1	2.457(1.689-3.575)	0.001*	1.09(0.901-2.10)	0.074
Swimming practice in rivers/ ponds	Sometimes	50.0	1		1
	Always	37.1	0.444(0.293-0.671)	0.074
Washing clothes/utensil in open water sources	Sometimes	54.7	1
	Always	45.3	0.537(0.221-0.937)	0.069
Dirty unclipping Fingernails	Always	30.1	1		1
	Sometimes	54.0	2.725(1.868-3.976)	0.001*	0.545(0.352-0.845)	0.023*
Existing of animals inside the house	No	32.3	1		1
	Yes	53.4	2.395 (1.636-3.507)	0.001*	1.048(0.981-2.639)	0.068

*Statistically significant at P<0.05; 1 = reference value; OR = odds ratio; AOR = adjusted odds ratio

Risk factors associated with the prevalence of Giardia lamblia

Additionally, univariate analysis was performed based on a single Giardia infection (Table 6). It was found that age, practice of defecation in open fields (OR= 2.094, 95% CI 1.184–3.704), eating unwashed fruits and vegetables (OR= 2.987, 95% CI 1.766–5.052), drinking from unprotected stream water (OR= 4.998, 95% CI 2.833–8.817), washing clothes/utensil in open water sources (OR= 2.082, 95% CI 1.292–3.538), dirty unclipping fingernails houses (OR= 2.137, 95% CI 1.292–3.535), and existing of animals inside houses (OR= 1.967, 95% CI 1.113–3.478) were a significant predictor of giardiasis. Logistic regression analysis confirmed that the practice of defecation in an open field (Adjusted OR= 1.473, 95% CI 0.830–2.522), drinking from unprotected stream water (Adjusted OR= 2.261, 95% CI 0.879–3.473), and eating unwashed fruits or vegetables (Adjusted OR = 1.238, 95% CI 0.133–2.425) were a significant risk factor for Giardia infection.

Table 6

Univariate and multivariate analysis of potential risk factors associated with Giardia lamblia among schoolchildren in rural communities of Taiz, Yemen.

Variables		Infected %	OR (95% CL)	P value	AOR (95% CL)	P value
Age	≤10	18.0	1		1
	>10	9.0	0.447 (0.233-0.860)	0.014*	1.403 (0.833-1.890)	0.074
Gender	Male	16.2	1
	Female	14.5	0.874(0.528-1.0447)	0.602
Parent’s educational status	educated	52.7	1
	Non educated	47.3	0.766(0.466-1.258)	0.291
Family size	>5	55.4	1
	≤ 5	44.6	0.751(0.456-1.236)	0.259
Washing hand before meals	Always	54.0	1
	sometimes	14.1	0.859(0.491-1.492)	0.583
Defecation habits	latrine	11.4	1		1
	Open field	22.7	2.094(1.184-3.704)	0.001*	1.473(0.830-2.522)	0.024*
Eating unwashed fruits and vegetables	Always	9.2	1		1
	Sometimes	23.1	2.987(1.766-5.052)	0.001*	1.238(0.0.133-2.425)	0.020*
Source of drinking water	Protected tap water	6.7	1		1
	Unprotected stream/well	26.5	4.998(2.833-8.817)	0.001*	2.261(0.879-3.473)	0.037*
Swimming practice in rivers/ ponds	Sometimes	14.8	1		1
	Always	17.5	0.759(0.442-1.303)	0.485
Washing clothes/utensil in open water sources	Sometimes	11.5	1		1
	Always	21.4	2.082(1.292-3.538)	0.004*	0.938(0.071-1.70)	0.084
Dirty unclipping fingernail	always	11.2	1		1
	Sometimes	21.3	2.137(1.292-3.535)	0.003*	1.041(0.301-1.9400	0.066
Existing of animals inside the house	No	12.0	1		1.
	Yes	21.3	1.967(1.113-3.478)	0.006*	2.24(0.932-3.12)	0.130

*Statistically significant at P<0.05; 1 = reference value; OR = crude odds ratio; AOR = adjusted odds ratio

Risk factors associated with the prevalence of Schistosoma mansoni

Regarding the behaviors possibly associated with Schistosoma mansoni among schoolchildren, practices such as defecation in open fields (OR = 1.017; 95% CI 0.173–2.947, P =0.041), swimming in rivers/ponds (OR = 2.471; 95% CI 1.667–3.046, P=0.001), and washing clothes/utensils in open water sources (OR = 2.473; 95% CI 1.260–3.865, P =0.013) were significantly associated with Schistosoma mansoni infection among schoolchildren. However, eating without washing hands (OR = 0.590; 95% CI 0.309–1.126, P = 0.106), eating unwashed fruits and vegetables (OR = 0.681; 95% CI 0.393–1.181, P = 0.170), drinking unprotected water (OR = 0.715; 95% CI 0.413–1.240, P = 0.213), and dirty unclipping fingernails (OR = 0.685; 95% CI 0.400–1.174, P = 0.167) were not significantly associated with Schistosoma infection. Multivariate analysis identified that practicing swimming in the river/ponds (adjusted OR = 1.826; CI 1.048–3.183; P = 0.034), and practicing open defecation, especially near water sources (adjusted OR = 2.383; CI 1.302–4.363; P = 0.005) as independent risk factors for Schistosoma mansoni infection among schoolchildren (Table 7).

Table 7

Univariate and multivariate logistic of potential risk factors associated with Schistosoma mansoni among schoolchildren in rural communities of Taiz, Yemen.

Variables		Infected %	OR (95% CL)	P value	AOR (95% CL)	P value
Age	<10	11.9	0.662(0347-1.265)	0.273
	>10	15.7	1
Gender	Male	16.2	1
	Female	14.5	1.175(0.688-2.007)	0.555
Parent’s educational status	educated	13.8	1
	Non educated	12.3	0.874(0.512-1.490)	0.620
Family size	>5	13.1	1
	<5	12.1	1.127(0.660-1.924)	0.661
Washing hand before eating	Always	13.4	1
	sometimes	12.0	0.590(0.309-1.126)	0.673
Defecation habits	latrine	11.1	1		1
	Open field	16.3	1.017(0.173-2.947)	0.041*	2.383(1.302-4.363	0.005*
Eating unwashed fruits and vegetables	Always	14.9	1
	sometimes	10.6	0.681(0.393-1.181)	0.170
Source of drinking water	Protected tap water	14.6	1
	Unprotected stream/ well	10.9	0.715(0.413-1.240)	0.231
Swimming practice in rivers/ ponds	Sometimes	9.4	1		1
	Always	15.8	2.472 (1.667-3.046)	0.011*	1.826(1.048-3.183)	0.005*
Washing clothes/utensil in open water	Sometimes	8.3	1
sources	Always	16.1	2.473 (1.260-3.865)	0.013*	2.73(1.79-4.015)	0.825
Dirty unclipping fingernail	Always	12.6	1
	Sometimes	11.3	0.784 (0.437-1.404)	0.412
Existing animals inside house	Yes	15.7	1
	No	11.3	0.685 (0.400-1.174)	0.167

* Statistically significant at P<0.05; 1 = reference value; OR = odds ratio; AOR = adjusted odds rati

Discussion

In low-income countries such as Yemen, IPIs remain a challenge to public health. Studies in different settings are essential for identifying and designing effective intervention mechanisms for high-risk communities.

IPIs are highly prevalent among children in rural schools in Taiz (51.26 %), with more protozoal infections than helminthic (30.3 vs. 20.92 %). The results are in accordance with those reported among 330 patients attending general and local hospitals in Taiz urban area, Yemen (Talal Al, 2016). In addition, IPIs have been reported at a higher rate among 1218 primary schoolchildren in rural communities of Sana’a (54.8 %) and 200 schoolchildren in Al-Mahweet governorate (90.0 %), northwest of Sana’a (Alwabr et al., 2016). Many other developing countries, including India (49 %), Nepal (51.9 %), Oshoidi Logos, Nigeria (58.3 %), and Burkina Faso (84.7 %), have reported a high prevalence of IPIs among school children (Sitotaw, B. et al.,2019). In rural areas of Peru (Choi et al., 2017), over 100 % prevalence rates were reported among schoolchildren, proving that IPIs remain a major threat to poor society. According to our study, the infection rate with intestinal parasites is higher than in studies conducted among schoolchildren from Saudi Arabia (27.8 %; Al-Mohammed et al., 2010), Egypt (30.7 – 33.6 %) (Abdel Fatah et al., 2012), and Oman (38.7 %) (Patel et al., 2006). Variations in geography, methodology (sample size, diagnostic methods, study participants), study setting, and study period could be potential reasons for the differences in prevalence. Among schoolchildren, 37.4 % had a single infection, whereas 4.4 % and 1.7 % harbored double and triple infections, respectively. According to Alsubaie et al., 2016, parasitic infection among children in Ibb was commonly due to a single parasite species. In contrast, infections due to multiple parasites was shown to be the most common among Al-Mahweet schoolchildren (75.5 %) (Alwabr et al., 2016).

This study found no association between gender and the rate of IPIs (P > 0.05) (Table 5). Earlier studies in Taiz (Al-Harazi, 2016), Sana’a (Alyousefi et al., 2011), and Al-Mahweet governorate, northwest of Sana’a (Alwabr et al., 2016), revealed similar findings.

However, there is substantial evidence that females are less likely to be exposed to IPIs than males (Abdi et al., 2017; Alsubaie et al., 2016; Hailegebriel, 2017) due to differences in gender roles. Age, on the other hand, was observed to be associated with IPIs (Table 5). Children as young as ten years old or less had a high prevalence rate. According to reports from various areas in Yemen, older children have a lower infection rate. Poor environmental sanitation and personal hygiene are frequently revealed as the main contributors to the increased prevalence of intestinal parasites among study participants (Table 5).

Risk factors associated with the prevalence of IPIs

Unwashed hands habits before eating, open field defecation behavior, eating unwashed fruit and vegetables, lacking safe drinking water, dirty unclipped fingernails, and the presence of animals inside their houses were found to be major risk factors for the prevalence of IPI among school children in this rural area (p < 0.05). These findings are consistent with previous studies performed elsewhere in Yemen, e.g. (Al-Harazi, 2016; Alyousefi et al., 2011). The degree of association between IPIs and other risk factors was determined by multivariate logistic regression (Table 5). Unwashed before eating, open field defecation, unwashed fruits and vegetables, and dirty unclipped fingernails were all identified as predictors of IPIs among the study’s participants. Participants who defecated in open fields were twice as at risk as those who defecated in latrines. On the other hand, students’ practices of washing fruits were found to be significantly related to IPIs. Compared to students who always washed fruits and vegetables, those who did not were three times more likely to become infected. Additionally, students who did not frequently clean and clip their fingernails were about three times as likely to develop IPIs as those who did. These results are consistent with those reported in other studies (Abossie et al., 2014; Gebretsadik, 2016; Hailegebriel, 2017).

Risk factors associated with Giardia lamblia

According to Table 2, about 15 % of students were infected with Giardia lamblia, followed by Entamoeba histolytica/dispar and Schistosoma mansoni. Logistic regression confirmed that open field defecation behavior, eating unwashed fruit and vegetables, and drinking unprotected water were all risk factors for Giardia lamblia infection. As a result, the risk of infection with Giardia lamblia was doubled in study subjects who defecated in open fields (OR = 2.094, 95% CI 1.184–3.704 P = 0.001), roughly threefold in those who ate unwashed fruits and vegetables (OR = 2.987, 95% CI 1.766–5.052 P = 0.001), and fivefold in those who drank from unsafe rivers and streams (OR = 4.998,95% CI 2.833–8.817 P = 0.001) compared with those who used latrine, not eating unwashed fruits and vegetables, and drank from unsafe rivers and streams (Table 6). Another study found that this parasite had a high prevalence among school children in Yemen (20 – 45 % and 30 – 35 %) and other countries (Alamir et al., 2013; Choy et al., 2014).

Schoolchildren of 10 years old or younger are significantly more likely to be infected with Giardia lamblia than those older than 10 years. This might be because they have relatively poorer personal hygiene habits. Meanwhile, schoolchildren from Hadhramout (16.8 %) and Ibb (14.0 %) had similar infection rates with Entamoeba histolytica/disorder dispar (55, 56). However, children from Al-Mahweet and Ibb recorded higher infection rates of 64.0 % and 33.7 %, respectively (Alsubaie et al., 2016; Alwabr et al., 2016).

Risk factors associated with the prevalence of Schistosoma mansoni

Among the study participants, the third most prevalent parasite was Schistosoma mansoni, with 13.0 %. Students’ swimming habits in rivers and ponds may account for this high prevalence rate. Additionally, open defecation or urination in or near water may have contributed to Schistosoma mansoni infection in study subjects (Table 7). An interesting finding was the absence of Schistosoma haematobium in the studied children. These results are consistent with earlier studies conducted in Taiz and other governorates (T. H. Alharazi et al., 2021; Alharbi et al., 2019; Al-Shamiri et al., 2011). In contrast, S. haematobium was found to be the predominant species in other governorates, such as Sana’a and Almahweet, rather than S. mansoni (Alwabr et al., 2016; Hany et al., 2015). This variance in species distribution may be explained by the occurrence of suitable freshwater snails that act as the necessary molluscan hosts (Rabone et al., 2019; Sady et al., 2013). In terms of gender, the current study demonstrated no statistically significant difference in schistosomiasis prevalence between male and female subjects. Furthermore, Sady et al., 2013 found that male children with schistosomiasis did not have a significantly higher infection rate than female children.

Of soil-transmitted helminths, only A. lumbricoides and T. trichiura were present with a low prevalence rate compared to studies carried out in Al-Mahweet (Alwabr et al., 2016), Ibb (Alsubaie et al., 2016), and Aden (Al-Abd et al., 2021). This may be attributed to the difference in educational levels and climates. Oppositely, hookworms and S. stercoralis were not found among schoolchildren in the current study. This is similar to reports from previous studies (Al-Qobati et al., 2012; bin Mohanna et al., 2014; MB, 2017; Singh Khadka et al., 2019; Sitotaw et al., 2020). However, hookworms and S. stercoralis have low prevalence rates in Ibb among schoolchildren, reporting 1.2 % and 0.8 % prevalence rates, respectively (Alsubaie et al., 2016).

Prevalence of Enterobius vermicularis, Ascaris lumbricoides and Trichuris trichiura

Although Enterobius vermicularis infections are easily persistent because of autoinfection, the current study found that the prevalence rate was low among rural students in Taiz (1.3 %). Generally, E. vermicularis infection was found in children from various Yemeni governorates at rates ranging from 0.8 % to 13.0 % (Al-Haddad et al., 2010; Al-Shibani et al., 2009; Alsubaie et al., 2016; Alwabr et al., 2016). In such a susceptible group, it is surprising that E. vermicularis were extremely low in prevalence. The low prevalence of E. vermicularis was probably due to the inadequacy of the coproparasitological techniques used to detect it.

One limitation of the study was the prevalence of infection with S. manasoni and soil-transmitted helminths instead of the intensity of infection. Reasons for this include the lack of resources and the unavailability of Kato-Katz kits on the local market. Additionally, stool specimens were obtained once from each participant, while conventional identification of intestinal parasites requires at least three specimens taken on three different days. Furthermore, due to security concerns, we selected only two rural districts in this governorate (Almawasit & Sabir Almawadim).

Conclusion

The high prevalence rates of IPI infection are a primary concern to public health in low-income neighborhoods where poor sanitation conditions, poor general health practices, inadequate toilet facilities, contaminated food and water, and malnutrition remain. G. lamblia, E. histolytica/dispar, and S. mansoni were among the intestinal parasites commonly found in schoolchildren. The most significant risk factors for these infections have been identified as practice unlashing hands before eating, open field defecation, drinking from unsafe water, eating unwashed fruits and vegetables, swimming in rivers or ponds, and having dirty unclipping fingernails. Political leaders must engage in concerted efforts to reduce intestinal parasitic infection rates.

Zahlen und Tabellen

Distribution of intestinal parasitic infections among schoolchildren in rural communities of Taiz, Yemen (2019 – 2020) according to age.

Parasite species	Age group (years)^a		P value
	≤10 n (%)	>10 n (%)
Protozoa
Giardia lamblia	62 (18.0)	12 (9.0)	0.014
E.histolytica/dispar/moshkovskii	58 (16.9)	13 (9.7)	0.061
Total	120 (34.9)	25 (18.7)	0.018
Helminths
Schistosoma mansoni	41(11.9)	21(15.7)	0.273
Ascaris lumbricoides	17 (4.9)	1 (0.8)	0.032^b
Trichuris trichiura	10 (2.9)	4 (3.0)	1.000^b
Enterobius vermicularis	5 (1.4)	1 (0.8)	1.000^b
Total	73(21.2)	27(20.2)	0.386

Univariate and multivariate logistic of potential risk factors associated with Schistosoma mansoni among schoolchildren in rural communities of Taiz, Yemen.

Variables		Infected %	OR (95% CL)	P value	AOR (95% CL)	P value
Age	<10	11.9	0.662(0347-1.265)	0.273
	>10	15.7	1
Gender	Male	16.2	1
	Female	14.5	1.175(0.688-2.007)	0.555
Parent’s educational status	educated	13.8	1
	Non educated	12.3	0.874(0.512-1.490)	0.620
Family size	>5	13.1	1
	<5	12.1	1.127(0.660-1.924)	0.661
Washing hand before eating	Always	13.4	1
	sometimes	12.0	0.590(0.309-1.126)	0.673
Defecation habits	latrine	11.1	1		1
	Open field	16.3	1.017(0.173-2.947)	0.041*	2.383(1.302-4.363	0.005*
Eating unwashed fruits and vegetables	Always	14.9	1
	sometimes	10.6	0.681(0.393-1.181)	0.170
Source of drinking water	Protected tap water	14.6	1
	Unprotected stream/ well	10.9	0.715(0.413-1.240)	0.231
Swimming practice in rivers/ ponds	Sometimes	9.4	1		1
	Always	15.8	2.472 (1.667-3.046)	0.011*	1.826(1.048-3.183)	0.005*
Washing clothes/utensil in open water	Sometimes	8.3	1
sources	Always	16.1	2.473 (1.260-3.865)	0.013*	2.73(1.79-4.015)	0.825
Dirty unclipping fingernail	Always	12.6	1
	Sometimes	11.3	0.784 (0.437-1.404)	0.412
Existing animals inside house	Yes	15.7	1
	No	11.3	0.685 (0.400-1.174)	0.167

Prevalence of intestinal parasitic infections among schoolchildren in rural communities of Taiz, Yemen (2019 – 2020).

Parasite species	Number positive	Percentage (%)
Overall	245	51.26
Protozoa
Giardia lamblia	74	15.5
E.histolytica/dispar/moshkovskii	71	14.9
Total	145	30.3
Helminths
Schistosoma mansoni	62	13.0
Ascaris lumbercoid	18	3.8
Trichuris trichiura	14	2.9
Enterobius vermicularis	6	1.3
Total	100	20.9
Single	179	37.4
Double	21	4.4
Triple	8	1.7

Distribution of intestinal parasitic infections among schoolchildren in rural communities of Taiz, Yemen (2019 – 2020) according to gender.

Parasite species	Gender^a Male n (%)	Female n (%)	P value
Protozoa
Giardia lamblia	44 (16.2)	30 (14.5)	0.602
E.histolytica/dispar/moshkovskii	41 (15.1)	30 (14.5)	0.846
Total	85 (31.4)	60 (29.0)	0.786
Helminths
Schistosoma mansoni	33 (12.2)	29 (14.0)	0.715
Ascaris lumbricoides	11 (4.1)	7 (3.4)	0.700
Trichuris trichiura	6 (2.2)	8 (3.9)	0.289
Enterobius vermicularis	3 (1.1)	3 (1.4)	0.739
Total	53 (19.6)	47 (22.7)	0.462

Socio-demographic characteristics of school children in rural communities of Taiz, Yemen.

Socio-demographic variables	categories	Frequency (n)	Percentage (%)
Age	≤10	344	72
	>10	134	28
Sex	Male	271	56.7
	Female	207	43.3
Parent’s educational status	literate	225	47.1
	illiterate	253	52.9
Family size	<5	236	49.4
	≥ 5	242	50.6
Washing hand before meals	Always	148	31.0
	sometimes	330	69.0
Defecation habits	Latrine	153	32.0
	Open field	325	68.0
Eating washed fruits and vegetables	Always	132	27.6
	sometimes	346	72.4
Source of drinking water	Protected tap water	147	30.8
	Unprotected stream/well	331	60.2
Swimming practice in rivers/ ponds	Sometimes	240	50.20
	Always	238	49.8
Washing clothes/utensil in open water sources	Sometimes	261	54.6
	Always	217	45.4
Dirty unclipping Fingernails	Always	144	30.1
	Sometimes	334	69.9
Existing of animals inside the house	No	258	54.0
	Yes	220	46.0

Univariate and multivariate analysis of potential risk factors associated with intestinal parasitic infections among schoolchildren in rural communities of Taiz, Yemen

Variables		Infected %	OR (95% CL)	P value	AOR (95% CL)	P value
Age	>10	31.3	1		1
	≤10	43.6	1.391 (1.054-1.837)	0.014*	0.903(0.210-1.524)	0.601
Gender	Male	39.1	1
	Female	41.5	1.106(0.765-1.600)	0.591
Parent’s educational status	educated	41.3	1
	Non educated	39.1	0.912(0.633-1.316)	0.624
Family size	>5	41.2	1
	≤ 5	39.0	1.102(0.764-1.589)	0.602
Washing hand before meals	Always	31.0	1		1
	sometimes	44.0	1.753(1.157-2.657)	0.008*	2.07(1.281-3.368)	0.013*
Defecation habits	Latrine	32.0	1		1
	Open field	54.7	2.558(1.741-3.757)	0.001*	1.869(1.216-2.874)	0.004*
Eating washed fruits and vegetables	Always	27.5	1		1
	sometimes	55.6	3.299(2.252-4.831)	0.001*	0.289(0.010-1.37)	0.011*
Source of drinking water	Protected tap water	30.7	1		1
	Unprotected stream/well	52.1	2.457(1.689-3.575)	0.001*	1.09(0.901-2.10)	0.074
Swimming practice in rivers/ ponds	Sometimes	50.0	1		1
	Always	37.1	0.444(0.293-0.671)	0.074
Washing clothes/utensil in open water sources	Sometimes	54.7	1
	Always	45.3	0.537(0.221-0.937)	0.069
Dirty unclipping Fingernails	Always	30.1	1		1
	Sometimes	54.0	2.725(1.868-3.976)	0.001*	0.545(0.352-0.845)	0.023*
Existing of animals inside the house	No	32.3	1		1
	Yes	53.4	2.395 (1.636-3.507)	0.001*	1.048(0.981-2.639)	0.068

Univariate and multivariate analysis of potential risk factors associated with Giardia lamblia among schoolchildren in rural communities of Taiz, Yemen.

Variables		Infected %	OR (95% CL)	P value	AOR (95% CL)	P value
Age	≤10	18.0	1		1
	>10	9.0	0.447 (0.233-0.860)	0.014*	1.403 (0.833-1.890)	0.074
Gender	Male	16.2	1
	Female	14.5	0.874(0.528-1.0447)	0.602
Parent’s educational status	educated	52.7	1
	Non educated	47.3	0.766(0.466-1.258)	0.291
Family size	>5	55.4	1
	≤ 5	44.6	0.751(0.456-1.236)	0.259
Washing hand before meals	Always	54.0	1
	sometimes	14.1	0.859(0.491-1.492)	0.583
Defecation habits	latrine	11.4	1		1
	Open field	22.7	2.094(1.184-3.704)	0.001*	1.473(0.830-2.522)	0.024*
Eating unwashed fruits and vegetables	Always	9.2	1		1
	Sometimes	23.1	2.987(1.766-5.052)	0.001*	1.238(0.0.133-2.425)	0.020*
Source of drinking water	Protected tap water	6.7	1		1
	Unprotected stream/well	26.5	4.998(2.833-8.817)	0.001*	2.261(0.879-3.473)	0.037*
Swimming practice in rivers/ ponds	Sometimes	14.8	1		1
	Always	17.5	0.759(0.442-1.303)	0.485
Washing clothes/utensil in open water sources	Sometimes	11.5	1		1
	Always	21.4	2.082(1.292-3.538)	0.004*	0.938(0.071-1.70)	0.084
Dirty unclipping fingernail	always	11.2	1		1
	Sometimes	21.3	2.137(1.292-3.535)	0.003*	1.041(0.301-1.9400	0.066
Existing of animals inside the house	No	12.0	1		1.
	Yes	21.3	1.967(1.113-3.478)	0.006*	2.24(0.932-3.12)	0.130

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Helminthologia

Intestinal parasitic infection among rural schoolchildren in Taiz, Yemen: School-based assessment of the prevalence and associated risk factors

T. Alharazi
T. Alharazi

Online veröffentlicht: 17 Dec 2022

Volumen & Heft: Volumen 59 (2022) - Heft 3 (September 2022)

Seitenbereich: 233 - 245

Eingereicht: 22 Dec 2021

Akzeptiert: 01 Sep 2022

Details zu Zeitschrift und Ausgabe

Helminthologia

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Artikel

Fig. 1

Zahlen und Tabellen

Fig. 1

Distribution of intestinal parasitic infections among schoolchildren in rural communities of Taiz, Yemen (2019 – 2020) according to age.

Univariate and multivariate logistic of potential risk factors associated with Schistosoma mansoni among schoolchildren in rural communities of Taiz, Yemen.

Prevalence of intestinal parasitic infections among schoolchildren in rural communities of Taiz, Yemen (2019 – 2020).

Distribution of intestinal parasitic infections among schoolchildren in rural communities of Taiz, Yemen (2019 – 2020) according to gender.

Socio-demographic characteristics of school children in rural communities of Taiz, Yemen.

Univariate and multivariate analysis of potential risk factors associated with intestinal parasitic infections among schoolchildren in rural communities of Taiz, Yemen

Univariate and multivariate analysis of potential risk factors associated with Giardia lamblia among schoolchildren in rural communities of Taiz, Yemen.

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Helminthologia

Intestinal parasitic infection among rural schoolchildren in Taiz, Yemen: School-based assessment of the prevalence and associated risk factors

T. AlharaziT. Alharazi

Online veröffentlicht: 17 Dec 2022

Volumen & Heft: Volumen 59 (2022) - Heft 3 (September 2022)

Seitenbereich: 233 - 245

Eingereicht: 22 Dec 2021

Akzeptiert: 01 Sep 2022

Details zu Zeitschrift und Ausgabe

Helminthologia

PDF-Vorschau

Artikel

Fig. 1

Zahlen und Tabellen

Fig. 1

Distribution of intestinal parasitic infections among schoolchildren in rural communities of Taiz, Yemen (2019 – 2020) according to age.

Univariate and multivariate logistic of potential risk factors associated with Schistosoma mansoni among schoolchildren in rural communities of Taiz, Yemen.

Prevalence of intestinal parasitic infections among schoolchildren in rural communities of Taiz, Yemen (2019 – 2020).

Distribution of intestinal parasitic infections among schoolchildren in rural communities of Taiz, Yemen (2019 – 2020) according to gender.

Socio-demographic characteristics of school children in rural communities of Taiz, Yemen.

Univariate and multivariate analysis of potential risk factors associated with intestinal parasitic infections among schoolchildren in rural communities of Taiz, Yemen

Univariate and multivariate analysis of potential risk factors associated with Giardia lamblia among schoolchildren in rural communities of Taiz, Yemen.

Referenzen

Neueste Artikel

Planen Sie Ihre Fernkonferenz mit Scienceendo

T. Alharazi
T. Alharazi