Abstract: Intestinal parasite infections are major public health problems of children. The study aimed to assess the prevalence of intestinal parasites and associated risk factors among preschool children in Riyadh city. Samples were obtained from 255 preschool children (157 girls and 98 boys), a single stool sample was collected and examined microscopically for the presence of intestinal parasites using a formalin-ether sedimentation technique. The overall prevalence of parasites was 45 (17.7%), the most of them had diarrhea 40 (15.7%) was a significant difference, (p<0.05). The prevalence rate of infection in boys and girls were (20.4%, 15.9%), respectively. In all preschool children, the highest infection rate was (23.3%) among the age group ranged between 3-5 years. The study detected about seven types of intestinal parasites among preschool children, the most common parasites were Giardia lamblia (37.8%). In this study the relationships were observed between intestinal parasitic infection and some of socio-demographic factors. Concerning the parents educational level was highly significant difference (p<0.001). Working mothers, presence of house maid, attending day care centers and poor hygienic measures and moderate socioeconomic standards were played role as predisposing factors for transmission of infection. The prevalence of infection with intestinal parasites between two different area in Riyadh was no significant. The study indicated that parasitic infections are important public health problems. Thus, infection control measures and the development of awareness strategies to improve sanitation and health education should be considered.
INTRODUCTION
Parasitic infections specially intestinal parasites which caused by helminths and protozoa are a major cause of inveterate infection in humans worldwide with appraise show that fully one quarter of the world’s population is infected (WHO., 1999). Intestinal parasites appear an important public health problem, particularly in developing countries where the climates is suitable for spread the intestinal parasites (Arani et al., 2008). The most countries of the tropical region which has more than 80% of all deaths annually are because of infectious and parasitic disease accounting for over 3 million deaths. Protozoan and helminthic intestinal infections were estimated to 3.5 billion people world wild, mostly children, present clinical symptoms (Keiser and Utzinger, 2010; Brooker et al., 2009).
Parasitic infection or infestation can occur in children of all ages. Infants, toddlers and very young children in day care settings are at risk for the parasitic disease called giardiasis that causes diarrhea and it spread through contaminated feces (CDC., 2014).
Incidence of parasitic disease is generally associated with an unhygienic environment, importation of infection from other countries and unsanitary habits of the people. Furthermore, most intestinal parasites have been associated with ill health particularly in children in some countries. Even though the overall advancement in sanitation, overall number of people with special indication to children infected with parasites worldwide is thought to be growing (Curtis et al., 2000; Azazy and Raja'a, 2003; Nissapatorn et al., 2005).
According to WHO (2010), Soil-Transmitted Helminths are the second leading cause of mortality in children of age less than six years who live in Africa. Around 1.45 billion persons in the world were infected with Soil-Transmitted Helminths (STHs) in addition, 5.19 million indicate associated morbidity in 2010 (Pullan et al., 2014; Hotez et al., 2014). The disease burden due to schistosomiasis was estimated 3.31 million during 2010. Out of 1.45 billion infections because of STHs, 438.9 were infected with hookworm, 819.0 million with A. lumbricoides and 464.6 million with T. trichiura (Pullan et al., 2014).
In the recent years, worldwide some countries demonstrated high incidence rates of intestinal parasites infection among children, the percentage were 38.7 in Oman (Patel and Khandekar, 2006), 19.8% in Nepal (Mukhiya et al., 2012), 84% in Colombia (Salcedo-Cifuentes et al., 2012), 27.5% in Brazil (Nobre et al., 2013), 18.4-28.8% in Iran (Nematian et al., 2004; Masoumeh et al., 2012), 89.6% in Argentina (Gamboa et al., 2014), 93% in Nicaragua (Munoz-Antoli et al., 2014) and 32.3% in Malaysia (Sinniah et al., 2014).
In Kingdom of Saudi Arabia there are various reports have been published indicates the presence of a prevalence rate on parasitic diseases in children, as reported by Bolbol et al. (1989) who found in his study that prevalence was 20.8% in Riyadh. Moreover in the study at Al-Baha region, the percentage were 21.1% (Al-Eissa et al., 1995) and the percentage was 33.8% in Jeddah (Al-Braiken, 2008).
As reported by Ramakrishnan et al. (2007) who found that intestinal parasites are frequently transmitted by low level of environmental and personal hygiene, contamination of food and drinking water and poor sanitary conditions in developing countries. Proper investigation of the parasitic etiology of diarrhea leading to prompt and effective management can help in decreasing the morbidity and mortality in such patients.
Intestinal parasitic infections are globally endemic and have been described as constituting the greatest single worldwide cause of illness and disease among preschool children. Parasitic infections are linked to poor health, contributing to economic instability and social marginalization.
This study aimed to assess the prevalence of intestinal parasites and associated risk factors among preschool children and identify the associated risk factors of intestinal parasitic infections among preschool children.
MATERIALS AND METHODS
Design: A quasi experimental design was used to conduct the study.
Setting: The study was conducted in two central areas (North and South) Riyadh city, Kingdom of Saudi Arabia.
Sample: A total of 255 under-five preschool children (157 girls and 98 boys) were participated in the study. The sample were collected from several health centers in Riyadh city Kingdom of Saudi Arabia. During the period from May 2013 to September 2013.
Tools of data collection
A pre-designed questionnaire: It designed by the researcher to elicit data on socio-demographic and risk environmental factors that leads to the infection.
A single stool sample: Data was collected from each child in labeled sterile plastic containers and transported to the laboratory. A stool specimen of each preschool child was examined microscopically for the presence of the type of intestinal parasites.
Specimens were fixed and tested with 10% formalin for 30 min (2-3 g fecal-1) and then concentrated by a formalin-ether sedimentation technique. Samples were examined as wet saline mounts and in iodine preparation for detection of protozoan oocysts, cysts, helminthic eggs and larvae (Chessbrough, 1998). Permanent stained smears were performed for intestinal coccidian parasites by the modified Ziehl-Neelsen technique according to Garcia et al. (1983) and modified trichrome stain according to Ryan et al. (1993).
Ethical clearance: The ethical considerations were addressed by treating positive individuals using standard drugs under the supervision of a doctor and nurse working at the centres. The objective of the study was explained to children parents and oral consent was sought from parents or guardians of the selected children during stool sample collection.
Statistical analysis: Chi-Square test was used to compare the difference in the prevalence of intestinal parasites among children presenting with diarrhea. Attention to children age and sex differences and risk factors were considered significant if p was less than 0.05 (Greenwood and Nikulin, 1996).
RESULTS
Of 255 examined stool samples of preschool children 45 (17.7%) revealed presences about seven types of intestinal parasites.
Table 1 illustrates that the majority of the positive samples were children their age ranged from 3-5 years (23.3%). There was no significant difference in the prevalence of parasites between boys and girls, although the number of positive girls is higher than the number yielded positive parasites in boys. Concerning the parents’ educational level, it was found that the majority (61.1%) of them graduated from primary school were highly significant (p<0.001). On the other hand the table showed that (20.8%) working mothers were a significant difference (p<0.01). Furthermore, it was clear that the majority (22.3%) had house maid and (42.1%) of the mothers were poor with significant (p<0.01).
Table 2 clarified that prevalence of intestinal parasites among girls more than boys. It was found that Giardia lamblia and Blastocystis hominis percentage (6.12%) was more common among preschool boys but Giardia lamblia (7.01%) was the most common among preschool girls and there was no statistical significant difference between the both sex in all Overall type of infection.
As shown in Table 3 the overall infection was (p<0.05) significant difference in association between the presence of intestinal parasites species and diarrhea among the preschool children. On the other hand, it was observed that Giardia lamblia was the most common cause of diarrhea (p<0.05).
| Table 1: | Socio-demographic distribution of preschool children |
| *Significant difference | |
| Table 2: | Prevalence of intestinal parasites among preschool children between boys and girls |
| Table 3: | Association between the presence of intestinal parasites and diarrhea among the preschool children |
| *Significant difference | |
| Table 4: | Prevalence of intestinal parasites among preschool children in two different area in Riyadh |
Table 4 shed light on the difference between the two regions (South and North) of Riyadh in relation to the prevalence of infection, it is clear that the percentage of infection species were more common in South Riyadh (19.1%) but there was no statistical significant difference between South and North region. However, the infection by Giardia lamblia was common in both regions.
DISCUSSION
In the present study, the prevalence of intestinal parasites among preschoolers was 17.7%. They had at least one parasite in their stools which is lower than that reported in children under five years age by Mbae et al. (2013) in Kenya (25.6%) and by Canete et al. (2012) in Cuba, the prevalence rate in his study was (71.1%). The present study as a recent prevalence was in agreement with some previous report from Saudi Arabia in Riyadh (20.8%) (Bolbol et al., 1989) and in Al-Baha (21.1%) (Al-Eissa et al., 1995). However, it is lower than that found in Jeddah (33.8%) (Al-Braiken, 2008) but it is higher than that recorded in Eastern province (9.3%) by Qadri et al. (1995). Also, it is in agreement with previous studies in other countries, in Iran (18.4%) (Nematian et al., 2004) and in Nepal (19.8%) (Mukhiya et al., 2012). On the opposite side, it is lower than that reported in Oman (38.7%) (Patel and Khandekar, 2006), in Iran (28.8%) (Masoumeh et al., 2012), in Brazil (27.5%) (Nobre et al., 2013), in Ethiopia (24.3%) (Yirgalem et al., 2014) and in Malaysia (24.6%) (Sinniah et al., 2014). However, it is more lower than that found in Yamoussoukro (47.4%) (Koffi et al., 2014), Morocco (51%) (El Fatni et al., 2014), Colombia (84%) (Salcedo-Cifuentes et al., 2012), Argentina (89.6%) (Gamboa et al., 2014) and Nicaragua (93%) (Munoz-Antoli et al., 2014). Furthermore, giving an overall prevalence of diarrhea as shown Table 3 in 40 of the sufferers (15.7%) is significant (p<0.05), this in agreement with (Yilmaz et al., 2008; Dogan et al., 2012; Hegazi et al., 2013; Koffi et al., 2014). On the other hand, this result incompatible with Bolbol et al. (1989) who said that diarrhea is not a major sign of parasitic infestation in 0.6-6 years old.
As shown in Table 3 the most common intestinal parasites identified among preschool children were Giardia lamblia 17 (37.8%), Entamoeba histolytica 11 (24.4%), Blastocystis hominis 9 (20%), Cryptosporidium parvum 4 (8.9%), Cyclospora cayetanensis 2 (4.4%), Ascaris lumbricoides 1 (2.2%) and Hymenolepis nana 1 (2.2%). The most of these parasites were recorded in children in other studies in Saudi Arabia (Al-Eissa et al., 1995; Qadri et al., 1995; Bolbol et al., 1989; Al-Braiken, 2008). In addition, it was reported in several studies around the world in children (Sayyari et al., 2005; Sharif et al., 2010; Mukhiya et al., 2012; Vahedi et al., 2012; Manganelli et al., 2012) specially in children under five years age (Canete et al., 2012; Mbae et al., 2013).
In this study, Giardia lamblia was the most common parasites detected in preschool children (37.8%) this result is in agreement with the study which was reported by Alkhalife (2006) in Riyadh, Zakai (2004) in Jeddah and Al-Eissa et al. (1995) in Al-Baha. In the Middle East, several studies were carried out to determine the prevalence of G. lamblia infection, indicating it to be a most common protozoan in children (Sharif et al., 2010; Ashtiani et al., 2011; Vahedi et al., 2012; Canete et al., 2012; Masoumeh et al., 2012). However, the prevalence rate detected in this study was higher than that previously reported for this parasite in Jeddah by Al-Braiken (2008). Moreover, there is a significant association between infection and diarrhea (p<0.05) (Al-Tukhi et al., 1993).
The second common parasite in this study was Entamoeba histolytica (24.4%) between infected children which in agreement with the findings of Al-Eissa et al. (1995) in Al-Baha, Al-Braiken (2008) in Jeddah, Patel and Khandekar (2006) in Oman. On the other hand, it was lower than that found in Taif, western Saudi Arabia (48%) (Al-Malki, 2014) and Yamoussoukro (22.55%) (Koffi et al., 2014).
The most common parasites found is Giardia lamblia and the next most common is Entamoeba histolytica which is similar that reported by Qadri et al. (1995) and Al-Eissa et al. (1995) in eastern province and Al-Baha, respectively.
In addition, Blastocystis hominis was also common infections in the study which found in (20%) but less than G. lamblia and E. histolytica. Some studies were carried out to determine the prevalence of B. hominis infection with percentage close to that recorded in this study (Al-Braiken, 2008; Sharif et al., 2010; Manganelli et al., 2012; Dogan et al., 2012).
The prevalence of Cryptosporidium parvum was (8.9%), this was in accordance with several studies (Yilmaz et al., 2008; Dogan et al., 2012; Vahedi et al., 2012). However, the prevalence of the infection is lower than that observed in a study of the same area which reported a prevalence of Cryptosporidium infection among immunosuppressed children less than 2 years (69.7%) (Sanad and Al-Malki, 2007) and in children in Jeddah, symptomatic (32%) and asymptomatic (4.7%) (Al-Braiken et al., 2003).
Infection with Cyclospora cayetanensis was (4.4%) which is similar that recorded by El Fatni et al. (2014) but it is slightly lower than that recorded in the previous studies from the same area (Al-Megrin, 2009, 2010) and in Jeddah (Al-Braiken et al., 2003).
On the other hand, Infection with Ascaris lumbricoides and Hymenolepis nana which found in the lowest prevalence-one case for each, this was in contract with other studies which found it with low rate (Patel and Khandekar, 2006; Al-Braiken, 2008; Al-Megrin, 2010; Sharif et al., 2010). However, it was found in a higher prevalence in Nicaragua (Munoz-Antoli et al., 2014) and in Malaysia (Sinniah et al., 2014).
Parasitic infection was related to protozoa in (95.6%) and intestinal worms in (4.4%) which in completely deal with Ashtiani et al. (2011) who found parasitic infection in Iran was (95.33 and 4.87%) by protozoa and helminths respectively and infection with protozoa parasitic is highly significant with diarrhea (p<0.01). On the other hand, it was in disagreement with Gelaw et al. (2013) who reported infection (13.2%, 26.9%) with protozoa and helminths, respectively.
Regarding the prevalence of intestinal parasites among preschool children and the association between the presence of parasites with diarrhea, Table 3 showed that there was a highly significant difference between the presence of intestinal parasites species and diarrhea among the preschool children especially G. lamblia (p<0.01).
As shown in Table 2 the prevalence of infection with intestinal parasites among boys and girls preschool children were 20.4 and 15.9%, respectively indicating that both genders are equally susceptible to infection (p>0.05). This result in agreement with many studies founded as in Thiland, the prevalence was (18.5%, 16.1%) (Wongstitwilairoong et al., 2007), in Italy (17.1%, 12.7%) (Manganelli et al., 2012), in Kenya (51.6%, 48.4%) (Mbae et al., 2013), in Wonji, Ethiopia (25.1%, 23.5%) (Yirgalem et al., 2014) and in Morocco (63.5%, 60.4%) (El Fatni et al., 2014) in boys and girls respectively. However, it was in disagreement with the study that founded in Nepal where the prevalence was (16.9%, 22%) (Mukhiya et al., 2012) in Brazil (26.1%, 30.3%) (Nobre et al., 2013), in northwest and southern Ethiopia (32.1%, 35.9%) (Gelaw et al., 2013), (80.6%, 81.4%) (Abossie and Sied, 2014) in boys and girls respectively. However, it was founded that no significant (p>0.05) concerning association between sexes and species of intestinal parasites.
This study report that the group of age between 3-5 years had the highest proportion of intestinal parasites infection (23.3%) as compared with the other age groups in cases (p>0.05) which was in agreement with Yirgalem et al. (2014) who recorded the highest infection between 3 and 4 years. On the other side, it was in difference with (Wongstitwilairoong et al., 2007) who found that the highest infection was between children age ranged from 2 and 3 years.
In this study relationships were observed between intestinal parasitic infection and some of socio-demographic factors. Concerning the parents educational level, it is found that the majority parents who have low level of education had risk of their children to acquire the intestinal parasitic infection than other household heads who had higher education level with high statistically significant difference (p<0.001). This is in agreement with Abossie and Sied (2014). Moreover, it was found that the majority of infected children with intestinal parasites who had working mothers (20.8%) with statistically significant difference (p<0.01), it is in approvement with (Nobre et al., 2013) and (22.3%) of them had house maid with statistically significant difference (p<0.01). In Saudi Arabia economic growth speedy and increasing in rate of women who are working out home which lead to importation of housekeepers, with a potential also for importation of disease. However, importation of these workers may also increase the importation of the intestinal parasites commonly found in their countries. Female housekeepers arriving in Saudi Arabia emanated mainly from tropical countries such as Indonesia, Sri Lanka, Bangladesh, Philippines, India and some of these workers have infection with various types of parasites and other diseases indigenous to their home countries. The spread of infection with one or more parasites in Asian female housekeepers was 46.5% of in Abha region (Al-Madani and Mahfouz, 1995). The community should be interested in safety of these workers which the nature of their work required being in close contact with family members specially children. In addition, it noted that the infection with intestinal parasites is common in preschool children attending day care centers but statistically no significant difference (p>0.05) (Lander et al., 2012; Pedraza et al., 2014). Regarding socioeconomic standards, of those who had intestinal parasites (42.1%) had poor family than other who had good and high income (p<0.01), the low per capita income family was strongly associated with an increased risk for an infection (Nobre et al., 2013).
As shown in Table 4 the prevalence of infection with intestinal parasites between two different area in Riyadh was show a high rate of infection especially in south of Riyadh where the infection was (19.1%) as compared with north of Riyadh (14.9%) with no significant association between infection rate and the area. It could be due to, people living close to animals. This result indicate that the educated and the economic level is an effective factor on infection with intestinal parasites (Masoumeh et al., 2012).
CONCLUSION
The high prevalence of intestinal parasitic infections among the preschool children indicated that parasitic infections are important public health problems. Thus, infection control measures and the development of awareness strategies to improve sanitation and health education should be considered.
ACKNOWLEDGMENTS
We would like to thank the nurses who helped in the collection of samples and information, specially pediatric nurses. Also, we thank all health care centers and the parents that participated in this study for their cooperation.