Prevalence of Intestinal Parasites among Children Attending Assiut University Children ’ s Hospital , Assiut , Egypt

| Intestinal parasitic infections in children still remain an important public health problems in developing countries including Egypt. Several environmental and socio-economic factors are responsible for their continued persistence in children. This study was conducted to determine the prevalence of intestinal parasitic infections among children attending Assiut University Children’s Hospital, Assiut, Egypt. In this cross-sectional study, a total of 260 stool samples were examined from outpatient children aged 4 months-15 years by direct fecal smear, formal-ether concentration and modified acid-fast staining technique to detect intestinal parasites. The prevalence of intestinal parasites in the children under study was 26.5%. Twelve species of parasites were detected. Giardia lamblia (10.4%) Microsporidia (5%) and Cryptosporidium spp. (2.3%) were the commonest protozoan parasites, while Hymenolepis nana (5.8%) and Capillaria philippinensis (1.5%) were the commonest helminthic parasites. Mixed infections were observed in 7.3% of the children (n= 19/260). The most common associated clinical manifestations with parasitic infection were bloody stool, pallor mucous membranes, mucous in stool, diarrhea, anorexia, abdominal pain, abdominal distention and flatulence. This study indicated that intestinal parasites prevalent among children aged four months to 15 years in Assiut, Egypt are a significant cause of morbidity in infected children. So, intervention programs, including health education, improved socio-economic conditions and environmental sanitation are required.

Many environmental, social and geographical factors are responsible for sustained persistence and the variation in the incidence and prevalence of intestinal parasites within and across the countries (Rao et al., 2006;Workneh et al., 2014).Some of these factors include poor sanitary conditions, unhygienic practices, absence of clean water, poor housing facilities and poverty (Amuta and Houmsou, 2009).The high prevalence rate occurs due to poor personal and environmental sanitation, poverty and low standard health services (Rashid et al., 2011;Gabbad and Elawad, 2014).These factors are responsible for most of the diseases and deaths in developing countries (Adamu et al., 2006).
Intestinal helminthes infections are most common in school age children (Sehga et al., 2010) and have been related with high risk of anemia, malnutrition, impaired physical developments which will have negative effects on the cognitive function and learning ability (Rashid et al., 2011).
In Egypt, intestinal parasitic infection in children is a common public health problem; in all governorates it was identified among infants, preschool and school children (Mansour et al., 2013).Though the reported prevalence rates in different parts of Egypt vary considerably from one study to another, however, nearly 27% of the children are suffering from intestinal parasites (Ibrahium, 2011).Various prevalence rates of E. vermicularis, S. haematobium, G. lamblia, H. nana, S. mansoni, A. lumbricoides, E. histolytica and A. duodenale have been reported among children by Zaghlool (2003), Bauomy et al. (2010) in Assuit Governorate, El-Masry et al. (2007) in Sohag Governorate, Ibrahium (2011) in Minia Governorate, Mohammad et al. (2012) in Damietta Governorate, Safar and Eldash (2015) in Al-Fayoum Governorate.For the development of good preventive and control measures, epidemiological studies are important to produce baseline data on the occurrence of parasitic infections.The aim of the study was to determine the prevalence of intestinal parasitic infections among children attending Assiut University Children's Hospital, Assiut, Egypt.

study aREa
This study was carried out in Assiut City, Capital of Assiut Governorate, located 375 km south of Cairo, Capital of Egypt.Assiut city, geographical position ranges from longitude 30º 45' to 31º 27' east and from latitude 26 º45' to 27 º45' north (Moatamed, 2005).Assiut University Children's Hospital in Assiut is the main hospital in Upper Egypt receiving children referred from other hospitals, health units and clinics of all governments in Upper Egypt.

study PoPulation and saMPlE CollECtion
In a cross-sectional study, 260 outpatient random children aged 4 month to 15 years, 158 were males and 102 were females participated in the study.They were divided into 4 age groups; four month -< 4 years, 4 -< 8 years, 8 -< 12 years and 12 -15 years.Informed consent was obtained from the parents of each child after a clear explanation.For each child, age, sex, residence, presence/absence of clinical symptomatology were noted.All children were subjected to clinical examination.Fresh stool samples were collected from each child in a clean, covered and labelled plastic container.All the specimens were immediately transferred to Medical Parasitology Department Laboratory, Faculty of Medicine, Assiut University to be examined.

ExaMination of thE saMPlEs
In order to detect the presence of intestinal parasites, a macroscopic examination of the stool samples was performed for the presence of mucus, blood and any segments or adult worm of helminthes, followed by a microscopic examination for the presence of cysts, eggs, oocysts and larvae.A direct examination of the samples was performed within 12 hours of the collection of sample.Direct examination includes wet mount preparation using saline and iodine, then the concentration method by the formal-ether technique (Cheesbrough, 2009).In addition, modified kinyoun's acid-fast staining (Parija, 2008) using alcohol fixed smear was done to detect parasites like Cryptosporid-

rESultS
Out of the 260 children under study, aged between four months and 15 years, 158 were males and102 were females and 69 of them were infected with one or more parasites.
The prevalence of infection was higher among females (29.4%) than among males (24.7%), but the difference was not statistically significant (p>0.05).Both males and females showed a statistically significant higher prevalence rate for single intestinal parasitic infection (21.6% and 17.8%, respectively) than for mixed infection (6.9% and 7.8%, respectively) (p<0.05)(Table 3).Giardia lamblia has the highest prevalence of protozoan infection among both sexes (5.8 % for females and 5.6% for males).Among the helminthes, H. nana has the highest prevalence among both sexes (12.7% for females and 8.8% for males).G. lamblia, Cryptosporidium spp., E. histolytica, H. nana, E. vermicularis and C. philippinensis showed high prevalence in females while Microsporidia and E. coli showed high prevalence in males with no significant difference (Table 4).The age group 12-15 years had the highest prevalence of intestinal parasites (34.5%) with no detected mixed infection followed by the age group 4 years -<8 years (30.2%) with 8.1% prevalence of mixed infection.The age group 4 month -<4 years (25.2%) had the highest prevalence of mixed infection (10.3%) while the age group 8 years -<12 years had the lowest prevalence of parasites (15.8%) with 0.9% prevalence of mixed infection.The results of the present study showed differences in overall prevalence rates among different age groups, but these differences were statistically insignificant (p>0.05).A significant difference between the single and mixed rates of intestinal parasitic infection was detected in age groups 4 -<8 years and 12-15 years (p< 0.05) (Table 3).The prevalence rate detected in this study may be due to continued poor personal hygiene, an inadequate supply of drinking water and low standard environmental conditions and waste disposal system within the study area.Nevertheless, higher prevalence rates of 41.9 % and 69.3% were detected in Assuit (Kotb et al., 2011).The prevalence of protozoan infection (21.9%) was higher than that of helminthes parasite infection (11.9%).Higher prevalence rates of protozoan infection have been reported in Egypt by many authors (Ibrahium, 2011;Kotb et al., 2011;Mohammad et al., 2012).The high prevalence of protozoan infection in this study suggests contamination of drinking water (Bhat et al., 2013).However, helminthes prevalence was higher in some reports from Egypt (El-Masry et al., 2007;Bauomy et al., 2010).
The rate of mixed double infections was 7.3%, which was much lower than previous reports from Egypt (El-Masry et al., 2007;Bauomy et al., 2010;Kotb et al., 2011).This might be explained by variation in the environmental and geographical conditions of the study localities.al., 2010).The high prevalence among older children is due to their higher activities and outdoor existence behaviour, which are favourable to get the infection (El-Masry et al., 2007;Pooja et al., 2014).At the same time, this result was inconsistent with some of the reports, which showed a higher positive rate among younger children in Assuit (Bauomy et al., 2010) and in Minia Governorate (The prevalence rate in children aged 9-12 years was 76.1%) (Ibrahium, 2011).
G. lamblia followed by Microsporidia showed the highest protozoan infections in this study.Higher prevalence rates of G. lamblia infection (19.2%, 15.2% and 14% respectively) were detected by other authors in Assuit (Hassan and Hany, 2001;Zaghlool, 2003;Bauomy et al., 2010).Even so, lower prevalence rates of infection were reported for other parts of Egypt (Abou El-Soud et al., 2009;Mohammad et al., 2012).Several species of Microsporidia have emerged as opportunistic agents in immunocompromised patients and have also been reported in immunocompetent patients (Tremoulet et al., 2004).The detected prevalence rate of Microsporidia in this study was nearly equal to previous studies in Assuit (4.2%) (Zaghlool, 2003) and Egypt (4.8%, 5%) (El-Mahallawy et al., 2011;Massoud et al., 2012).During the present study, E. coli, Cryptosporidium spp.and E. histolytica were reported in 2.7%, 2.3% and 1.5%, respectively.Similar and lower prevalence rate of Cryptosporidium spp (2.5%, 0.4%0) were reported in Assuit (Shaheen, 1992;Zaghlool, 2003).The prevalence rate of E. histolytica detected in the present study was lower than that reported in previous studies in Assuit (10.8%, 5%) (Hassan and Hany, 2001;Zaghlool, 2003) and Egypt (Stauffer et al., 2006;El-Masry et al., 2007;Abou El-Soud et al., 2009;Mohammad et al., 2012).Because all protozoan infections detected in this study spread by direct fecal-oral passage or by food borne or water borne transmission, these differences of prevalence in different locations may be attributed to different levels of sanitation, types of water supply, hygienic measures and food behaviors (Bauomy et al., 2010).
H. nana was the commonest helminthes (5.8%) detected in this study with most of the cases between ages 4 and 8 years.Children between ages 4 and 10 years and those living in bad hygienic conditions which favor spread by autoinfection are the most frequently affected by H. nana (Macariola et al., 2002).C. philippinensis was the second common helminthic infection detected in this study (1.5%  et al., 2000).
The same prevalence rate of A. lumbricoides, Fasciola spp.(0.8%) was detected during the present study, which is similar to previous study in Assiut (Zaghlool, 2003) but lower than other studies in Egypt (Hassan and Hany, 2001;Abou El-Soud et al., 2009;Mohammad et al., 2012).The prevalence of E. vermicularis (0.8%) found in the present study could be underestimated because it was not systematically detected by using the cellophane tape smear method which has higher sensitivity than stool examination (González-Moreno et al., 2011).
Early identification of abdominal symptoms can help us to identify the presence of parasites ( Jayarani et al., 2014).
The positive association between some clinical manifestations and parasitic infections was detected in this study, including bloody stool, mucous in stool, pallor mucous membrane, diarrhea, anorexia, abdominal pain, abdominal distention and flatulence.cOncluSIOn Although the prevalence rates of intestinal parasites in this study were nearly comparable with similar studies conducted in other regions in Egypt, the rates of infections are, however, of public health importance.Early identification of some reported clinical manifestations may help in the early detection of parasitic infection and effective treatment.Necessary sanitary strategies, health education, improvements of socio-economic conditions, screening and de-worming of intestinal parasites among children are recommended.

EthIcAl clEArAncE
This study was approved by the Institutional Ethics Review Board of the Faculty of Medicine, Assiut University, Assiut, Egypt.Oral consent was obtained from the patients before they were recruited into the study.

table 1 :
Prevalence of intestinal parasites among the 260 children under study

table 3 :
Prevalence of single and mixed intestinal parasites in relation to sex and age groups among the 260 children under study no examined Single infection no (%) Mixed infection no (%) total infected no (%) P. value *: Significant difference (p<0.05)The Journal of Advances in Parasitology October 2016 | Volume 3 | Issue 4 | Page 128

table 4 :
Prevalence of different intestinal parasites in relation to sex and age groups among the 260 children under study *: Significant difference (p<0.05)G.lambliaand Microsporidia showed significant high prevalence in the age group four month -<4 y while H. nana showed significant high prevalence in the age group 4 -<8 y (p<0.05)(Table4).The common clinical features of
). C. philippinensis is an emerging parasite in Egypt.Infection reports in children were scarce.Two sisters aged 8 and 12 years from El-Minia governorate were reported(El-Karaksy et al., 2004)while two boys aged 9 years old were reported from Assiut governorate(Attia et al., 2012).S. mansoni and A. duodenale showed the same prevalence rate (1.2%) in the present study.The prevalence of S. mansoni was low in this study but higher than that reported in other previous studies in Assuit (0.75%)(Hassan and  Hany, 2001)and in Damietta (0.9%)(Mohammad et al.,  2012).While two other current studies conducted in Assuit did not detect the presence of S. mansoni(Bauomy et  al., 2010; Kotb et al., 2011).The general decline in schistosomiasis rates Egypt in recent decades is apparently due to the intensive schistosomiasis control, and water supplies programs(Bassey and Umar, 2004).All infected children in the present study were males.Schistosomiasis is usually more prevalent among boys as boys have more frequent and unrestricted access to canal water than girls (El-Khoby