Intestinal parasitic infection among school children in Dakahlia governorate, Egypt: a cross-sectional study

Abstract

Background

Intestinal parasitic infections are still representing a significant health problem in developing countries including Egypt. School children are highly vulnerable to this type of infection, and they suffered many health consequences. This study was conducted to identify the prevalence of intestinal parasitic infection among school children and its related factors.

Results

This is a school-based cross-sectional study conducted on 726 school children selected from primary, preparatory, and secondary schools located at Aga district, Dakahlia governorate. A questionnaire sheet including data on the socio-demographic characters of students and their families, environmental and behavioral variables, and gastro-intestinal symptoms was filled. Also, fresh stool samples were collected from each child for microscopic examination to detect eggs, cysts, and trophozoites of intestinal parasites. There were 239 of 726 children with IPIs representing an overall prevalence of 32.9%. The most prevalent parasitic species were E. histolytica (12.3%), G. lamblia (8.5%), H. nana (7.7%), and A. lumbricoides (5.7%). There were significant differences between infected and non-infected children regarding age, educational stage, residence, monthly family income, and maternal education levels. Also, there were highly significant differences between infected and non-infected children regarding all environmental and behavioral variables and the occurrence of GIT symptoms.

Conclusion

High prevalence of IPIs among school children indicates little personal hygiene and poor environmental sanitation. Much more efforts are needed for the application of proper prevention and control strategy.

Background

Intestinal parasitosis is a group of diseases caused by infection by one or more cestodes, trematodes, nematodes, and protozoa [1, 2]. Health services have achieved significant improvement in the diagnosis and treatment of the parasitic disease; however, it still represents a challenge for health staff and facilities in many developing countries and IPIs infection is one of the major public health problems and affecting primarily school children [3]. The problem of IPIs is greater in poor countries with limited resources [4].

Parasitic infection is much more prevalent among poor individuals of the population. This is due to the associated poor housing conditions, poor personal hygiene and unsanitary environmental conditions, overcrowding, higher contact with contaminated soil and water, and lack of accessible health services [5]. It is also affected by behavioral, environmental, biological, socio-economic, and health service factors. Family income, educational and employment status, and quality of civil infrastructures have a role in disease transmission and the associated morbidity and even mortality [6, 7].

Most of the intestinal parasites are transmitted to their susceptible host by ingestion of contaminated foods and drinks or by getting in contact with contaminated soil and water where infection occurs through skin penetration by the infective larva stage. Sometimes, the infection may be acquired by close personal contact especially between school children [8].

Parasitic infection is associated with intestinal bleeding, nutritional deficiency, cell and tissue damage, anemia, and delayed physical and mental development. This leads to high rates of school absenteeism and poor academic performance [9,10,11].

Children are at high risk of infection due to their little awareness, immature immune system, and high nutritional requirements [12]. Children’s IPIs are significantly associated with wasting and stunted growth [13]. Therefore, World Health Organization (WHO) recommends periodic treatment of school children with anti-helmentic drugs especially in highly infected localities, and to improve the children’s nutritional status, hemoglobin, cognition, and overall health status [10].

In the last few years, the prevalence of IPIs and their associated risk factors among Egyptian school children were assessed through studies conducted in different governorates which revealed IPIs still representing a public health problem as it affects a considerable proportion of children. Therefore, periodic assessment of IPIs prevalence and identification of the associated risk factors is necessary for proper planning and implementation of effective prevention and control measures.

Therefore, the present study was performed to assess the prevalence of IPIs and identification of the possible related factors among school children in the Aga district of Dakahlia governorate.

Methods

Study design and setting

This is a school-based cross-sectional study that was conducted on primary, preparatory, and secondary school children in Aga district, Dakahlia governorate during the studying year 2020-2021from October 2020 to January 2021 to assess the prevalence of IPIs among school children. Dakhalia governorate is located in the northeast of the Delta region with an estimated population number 6.577 million. The capital of the governorate is Mansoura city which lies at a distance of 130 km of Cairo. Aga district lies 15 km south of Mansoura city at latitude 30.91° N and longitude 31.29° E with a population number 538.484 in July 2017 [14].

Sampling technique and sample size

A cluster sampling technique was used in the study where a school list in the Aga district was obtained from the local educational directorate. Schools were categorized according to their localities into urban and rural schools and from each category we selected randomly one school from each educational stage (primary, preparatory, and secondary). In the end, we have six schools; three urban (primary, preparatory, and secondary) and three rural (primary, preparatory, and secondary schools). A representative random sample of children was selected from each school which ranges from 10 to 15% of the total number of children in the school.

The calculated sample size required to perform the study was 367 children based on estimated IPIs prevalence 39.5% [15], 95% confidence interval, and 5% marginal errors. In order to increase the power of the study, we decided to double the calculated number, so the planned sample size was 734 children. During the data collection phase, 8 children failed to give stool samples, so we have complete data of 726 children who were included in the final analysis.

Study questionnaire

Data were collected using a structured questionnaire which was designed after reviewing the literature of similar objectives. It was prepared first in the English language and then translated to the Arabic language. Two staff members from parasitological and community medicine departments, Al-Azhar faculty of medicine assessed the quality of the questionnaire where some modifications were performed. Also, a pilot study was performed on 30 school children to assess its applicability. These students would not be included in the study. The questionnaire includes data on the socio-demographic characters (age, gender, educational stage, residence, monthly family income, and father and mother education) of the participants, environmental and behavioral risk factors (home environment, finger hygiene, handwash habit, washing vegetables and fruits well before consumption, domestic animal and water contact, and walking bare footed), and GIT symptoms (anorexia, nausea or vomiting, abdominal pain, bloating, constipation or diarrhea and bloody stool).

Data collection

Data collection was performed by three interviewers who were trained by the authors on the procedures of data collection and the method of stool sample collection and preservation. The selected children were interviewed to obtain information about their address and the mobile of their parents. Also, children received dry, clean, leak-proof, and labeled plastic disposable containers for stool sample collection. The questionnaire was filled out through home visiting of the selected children and interviewing their parents. During the interview, the home environment and fingernails hygiene of children were observed by the interviewers. At the end of the visit, a stool sample was collected.

Stool examination

In the laboratory, each collected sample was examined using a direct wet mount and the formal ether concentration technique. Stool specimens were examined macroscopically and microscopically. Stool samples were examined macroscopically and microscopically by (i) direct wet smear method [16], (ii) concentration methods by simple floatation and formol ether sedimentation techniques [17], and (iii) Kato-Katz technique [18]. The cellophane tape adhered to a glass slide was used by children to investigate the infection status of Enterobius vermicularis.

Data analysis was performed using the SPSS software version 20. Descriptive statistics in the form of frequencies and percentages were performed and the differences between the studied variables were analyzed using chi-square and Fisher’s exact tests. P value < 0.05 was considered a sign of significance.

The study was approved by the Ethics Committee of the Faculty of Medicine, Al-Azhar University. All the study participants and their parents were informed about the aim and the procedures of the study. Also, written informed consents were obtained from the parents before data collection. Permission from the responsible authorities to perform the study was obtained.

Results

There were 239 students infected with intestinal parasites of 726 studied students representing a prevalence rate of 32.9%. Of those infected students, there were 143 students mono-infected, 71 double-infected, and 25 triple-infected. The most prevalent parasites were E. histolytica/dispar (12.3%), G. lambilia (8.5%), H. nana (7.7%), and E. vermicularis (6.8%) (Table 1).

Table 1 Prevalence of intestinal parasitic infection among studied school children

The studied sample consisted of 385 (53.0%) male and 341 (47.0%) female children. There were 256 (35.3%) children with an age range between 6 and 10 years, 271 (37.3%) with age range 11–14 years, and 199 (27.4%) with age range between 15 and 18 years. Also, there were 336 children (46.3%) from rural areas whereas 390 (53.7%) were from urban areas. There were 151 (20.8%) children with family income less than 2000 L. E, 364 (50.1%) with family income between 2000 and 4000 L. E and 211 (29.1%) with family income more than 4000 L.E. Most of the children’s parents were of secondary level education (36.9% of fathers and 38.8% of mothers). Also, most of the infected children were male (53.0%), between 6 and 10 years old (35.3%), at primary school (40.1%), rural residents (53.7%), with family income between 2000 and 4000 L. E (50.1%), and secondary educated fathers and mothers (36.9% and 38.8%, respectively). There were significant differences between infected and non-infected children regarding gender, residence, family income, and mother’s educational level (Table 2).

Table 2 Socio-demographic risk factors of parasitic infection among studied school children

Most children have a clean home environment (66.4%), good hygiene of the fingernails (68.5%), wash their hands before and after meals (55.0%) and after bathroom use (57.3%), and wash vegetables and fruits well before consumption (61.0). On the other side, the minority of children has contact with domestic animals (32.6%), water contact activities (24.4%), and walks barefooted (25.5%). Also, most of the infected children have a dirty home environment (57.7%), bad fingernails hygiene (50.7%), not wash their hands before after meals (56.1%), not wash their hands after bathroom use (51.0%), not wash vegetables and fruits well before consumption (64.0%), in contact with domestic animals (65.7%), have water contact activities (60.0%), and walk barefooted (54.8%). There were highly significant differences between infected and non-infected children regarding all behavioral and environmental risk factors (Table 3).

Table 3 Environmental and behavioral risk factors of parasitic infection among studied children

The most-reported GIT symptoms among infected children were abdominal pain (60.7%), constipation or diarrhea (42.7%), bloating (38.5%), anorexia (30.1%), and nausea or vomiting (24.7%) whereas the presence of blood in stool was the least reported symptom (13.0%). These symptoms were much less prevalent in non-infected children. Also, highly significant differences were observed between infected and non-infected children (Table 4).

Table 4 Prevalence of GIT disorders among infected and non-infected children

Discussion

This study was conducted to identify the prevalence of different parasite species and the related factors among the most vulnerable group in the community; school children. This will aid to identify the hot infection areas and proper application of control measures.

There were 239 school children have positive results for parasitic stool analysis representing an overall prevalence of 32.9%. Of those infected children, there were 143 (19.7%) mono-infected children, 71 (9.8%) double infected, and 25 (2.3%) triple infected. This indicates parasitic infections still represent a public health problem among school children who are forming a considerable proportion of the population. This can be attributed to the unsanitary environmental conditions and low level of public awareness [19]. Egyptian studies conducted on school children revealed marked variability regarding the prevalence of IPIs with an infection range from 22.4 to 63.8% [15, 20,21,22,23,24,25,26,27,28,29,30,31].

The most prevalent parasitic species were E. histolytica (12.3%) and G. lamblia (8.5%). E. histolytica infection is strongly associated with drinking water sources contamination, poor personal hygiene, and lack of regular handwash habits [19]. Also, G. lamblia was associated with open field defecation, poor hand washing, raw vegetables, and unwashed fruit consumption [32]. This finding agreed with the findings of some Egyptian studies [20, 21, 24, 30] where E. histolytica was the most prevalent parasitic species with variable prevalence rates. However, other studies have shown variability regarding the most prevalent parasite where it was G. lambilia [15, 29], A. lumbricoides [25], and E.vermicularis [22, 26]. This variability regarding the overall prevalence of IPIs, type of infection, and parasite species can be attributed to different research settings and different characteristics of participants regarding socio-demographic, behavioral, and environmental characteristics. Also, the availability and quality of health services is an additional factor. Moreover, the different laboratory techniques used for parasitological diagnosis may have a role in this variable prevalence.

Also, variable findings were observed between studies conducted in Saudi Arabia [33,34,35] with prevalence rates 17.7%, 57.4%, and 5.3%, respectively. However, the most recent and powerful study [35] revealed a marked reduction in the prevalence of intestinal parasitic infection (5.3%) indicating improvement in the socio-economic and environmental conditions, personal hygiene and awareness, and the provided health services.

Similarly, much more variability was observed between Ethiopian studies [19, 32, 36,37,38,39] with prevalence rates ranging from 21.5 to 84.3%. Also, a systematic review and meta-analysis study [40] was conducted to identify the epidemiology of intestinal parasitic infection among preschool and school-aged children which included 83 studies from 1997 to 2019 and examined 56,786 stool specimens. It revealed that the prevalence of parasitic infection was 48% (95% CI: 42–53%) and the infection trend decreased by 17% (95% CI: 2.5–32%) every 6 consecutive years. This high prevalence of parasitic infection indicates bad environmental sanitary conditions and a low level of personal hygiene and awareness.

There were significant differences between infected and non-infected children regarding age, educational stage, residence, monthly family income, and mother’s educational level. Despite male students constitute most of the infected children (53.0%). However, there is no significant gender difference regarding IPIs (P=0.5). There were variable findings between Egyptian studies regarding gender differences where some studies [22, 23, 27, 28, 31] revealed similar findings with insignificant gender differences while other studies [21, 25, 29, 30] revealed significant gender differences. However, despite this variability, all of these studies except one [25] revealed a higher prevalence of IPIs among male students. This can be explained by their marked outdoor activity with more exposure to infectious pathogens. Also, insignificant gender differences were observed in studies conducted in Saudi Arabia [33,34,35] and in some Ethiopian studies [19, 36, 39].

Also, there is a highly significant difference between infected and non-infected children regarding their age. Children of the age group between 6 and 10 years have the highest prevalence of IPIs (46.6%) whereas other age groups (11–14 and 15–18 years) have lower prevalence (36.4% and 18.0%, respectively). This may be due to risky behavioral activities, little hygiene, and awareness of small age students about prevention and control measures in comparison with bigger age groups [32]. Similar findings were observed in other Egyptian [20, 21, 25] and Ethiopian studies [38, 39]. Also, primary school children have a higher prevalence of IPIs (55.7%) than preparatory and secondary school children (28% and 16.3%, respectively) with highly significant differences. This finding agreed with the finding of Workneh et al. [37] and Dessie et al. [38] where there were significant associations between the grade level of children and IPIs with a higher probability of infection among low-grade children. They attributed this association to behavioral factors and little children’s understanding of disease processes. Also, lower grade students have less developed immunity towards parasitic infection. However, the effect of age as an additional and confounding variable cannot be excluded.

There is a highly significant difference between infected and non-infected children regarding residence where most of the infected children were rural residents (61.1%). Similar findings were observed in other Egyptian studies [15, 23, 31]. Rural children mostly have risky behavior such as walking poor footed, water and domestic animal contact, poor fingernails and hand hygiene, and defecation in the open agricultural field which consequently leads to more soil contamination with parasites [15].

Also, a highly significant difference was found between infected and non-infected children regarding family income where most of the infected children were belonging to families with a monthly income of fewer than 4000 L. E (73.7%). Low-income families mostly have poor housing conditions with overcrowded and unsanitary housing conditions, malnourished children, and less educated parents and consequently have less personal hygiene and little awareness of parasites prevention and control measures. A similar finding was found by Hailegebriel [19] where the probability of parasitic infection among low-income family children was six and half times children from high-income families. However, insignificant findings were observed in similar studies [35, 36]. This may be due to statistical reasons such as a small sample size or a little number of infected children which was insufficient to give statistically significant findings [35].

Concerning parental education, there is a significant difference in IPIs of children regarding mothers’ education only (P=0.02). This indicates that mothers are more influential in preventing parasitic infections among their children. This is due to a longer time of contact with their children contrary to fathers who spend most of their time outside doors. The educated mother has more awareness about parasitic infection prevention and control and their impact on their children and consequently more able to protect their children. A significant effect of the mother’s education was observed in similar studies [21, 25, 41]. However, some studies [20, 33] revealed significant differences between infected and non-infected children regarding both fathers’ and mothers’ educations while other studies [35, 37] have found no significant differences.

Regarding the behavioral and environmental factors, there were highly significant differences between infected and non-infected children regarding these factors with a considerable proportion of children having an unsanitary environment, little fingers hygiene, poor hand washing practice, and risky health behavior. These findings explain the high prevalence of parasitic infection among studied children which indicates improper implementation of prevention and control measures that are effective in reducing the IPIs such as the provision of safe drinking water, proper sewage and refuse disposal, improvement of personal hygiene and environmental sanitation, increased public health awareness, and community involvement activities [42].

There were highly significant differences between infected and non-infected children regarding the GIT disorder with much more prevalence among infected children and highly significant differences (p <0.00001). These findings agreed with findings of similar studies [19, 23, 28, 30]. However, the presence of GIT symptoms can be helpful for the early detection of parasitic infections.

Study limitations

The following limitations may be considered when interpreting the study findings: (i) the study was conducted in a single locality (Aga district) in Dakahlia governorate. So, the generalization of the findings to other localities of the governorate or overall Egypt must be taken with caution. However, to increase the power of the study and its repetitiveness we increase the sample size by approximately 100% of the calculated sample. Also, being a cross-sectional study conducted at one point of time, seasonal variation in the children’s IPIs cannot be detected. (ii) Diagnosis of children’s IPIs was carried out by taking a single stool sample from each child. However, stool samples were checked by an associate professor in the field of medical parasitology (second author) to minimize the possibility of misdiagnosis. (iii) Antigen test to differentiate between E. histolytica and E. dispar was not carried out.

Conclusions

This study reveals that IPIs still have a high prevalence among school children with a considerable proportion of infected children being multi-infected. E. Histolytica and G. Lambilia were the most prevalent parasites. Socio-demographic factors related to parasitic infection were age, stage of education, residence, monthly family income, and maternal education. Also, there were highly significant differences between infected and non-infected children regarding all environmental and behavioral risk factors. Also, there were highly significant differences between infected and non-infected children regarding the prevalence of GIT symptoms. The study findings revealed the urgent need for IPIs prevention and control measures through an organized multi-sectoral complementary approach that involves policy-makers, health and educational organization, community and religious leaders, and mass media to increase the public awareness about IPIs, personal hygiene, environmental sanitation, and provision of accessible health services.