Prevalence of intestinal parasites among children referred to Children’s Medical Center during 18 years (1991–2008), Tehran, Iran

Abstract

Epidemiological studies show that parasitic inections are among the most common infections and one of the biggest health problems of the society worldwide. Children at school age have the highest morbidity compared with other ages. Therefore, by treating these children, the disease burden in the total population is reduced. In this study, prevalence of parasitic infection in children referred to Children’s Medical Center was compared in different years. In this retrospective cross-sectional study, the subjects were children under 13 years who were referred to Children’s Medical Center Laboratory during 18 years (1991–2008) and underwent stool exam by any reason. The specimens were evaluated by different common methods of stool parasitology. In suspected cases, parasites was cultured in specific medium and stained as needed. Required data were obtained from the laboratory files and analysed according to study’s purpose. Subjects were 124 366 children. Among them, 0.78% of cases had parasitic infections and 60.54% cases were male. Parasitic infections were related to protozoa in 95.33% cases and intestinal worms in 4.87%. Of them, 50.352% were pathogenic protozoa. The most parasitic infection was Giardia lamblia. Among intestinal worms, the highest prevalence was related to Hymenolepis nana (40.7%). A comparison between the first 10 years and the next 8 years of the study showed that the prevalence of intestinal parasites were 8% and 1% (P<0.001) and the rate for protozoal infection were 14.9% and 4.3%, respectively (P<0.001). The prevalence of intestinal parasites was reduced during recent years; however, more attempts should be performed to make it lower.

INTRODUCTION

Intestinal parasitic infections are one of the biggest socioeconomic and medical problems. Epidemiological studies show that parasitic infections are among the most common infections and one of the biggest health problems of the society worldwide. Surveys on the prevalence of various intestinal parasitic infections in different geographic regions are a prerequisite for developing appropriate control strategies. Research carried out in different countries has shown that the socioeconomic situation of the individuals is an important cause in the prevalence of intestinal parasites (Jamaiah and Rohela, 2005).

Two epidemiological factors distinguish parasitic diseases from other infections. The first factor is high prevalence of these infections so that parasitic infection prevalence estimates to be about 3–3.5 billion people, which cause 450 million deaths every year ( Lai, 1992; WHO, 1998; Markell et al., 1999). The second factor is the high rate of incidence in poor and disadvantaged communities which is specially seen in school-aged children (Nematian et al., 2004). These infections cause serious damage to children’s development in non-developed countries and are related to failure to thrive, reduced physical activity and learning power.

As described before, children at school age has the highest rate of morbidity because of intestinal parasites as compared with other ages (Nematian et al., 2008). Statistics shows that by treating these children, the disease burden in the total population is reduced to 70% which is significant (Lai, 1992). The main symptoms of the diseases are related to gastrointestinal. It may also cause anaemia, physical and mental problems such as delayed growth in children, weight loss, fatigue and itching or rash around the anus and vulva. Several studies have been carried out to find the prevalence of intestinal parasites among children and based on the geographical and health status of the study setting the findings differ. In this study, prevalence of parasitic infection in children referred to Children’s Medical Center was compared in different years.

MATERIAL AND METHODS

Study Design

In this study, the data were obtained from parasitology laboratory files and were ultimately analysed based on the study purposes.

In a retrospective approach, the study was conducted on referred children to Children’s Hospital Medical Center, from 1991 to 2008.

Subjects were children aged less than 13 years old who underwent stool exam. Considering that Children’s Medical Center is a referral centre for subspecialty services in the country, so through this investigation, valuable information was obtained about epidemiologic pattern of sex distribution and species of the organism causing diarrhea.

Criteria for Selecting the Sample

Stool exam records of 124 366 children who were referred to Children’s Hospital Medical Centre Central Laboratory were reviewed. As a routine, physicians order stool exam on 3 different days for maximum recovery of parasites. Stools were investigated through different methods of parasitology consisting of concentration, wet preparation and iodine preparation (Stoll et al., 1983; Alles et al., 1995, Idris and Al-Jabri, 2001). In all specimens, the stool was combined with a drop of saline and a drop of Logul, and was checked with light microscope. In formed samples, this procedure was carried out through concentration method (formalin ether method) in which the protozoan cyst and worm ovum are sought in larger amount of stool. Uncertain cases were confirmed by culture in specific medium for parasite (for example, amoeba culture in coagulated serum medium). If needed, specific staining (Trichrome) was confirmed. Other methods consisted of scotch test for Oxyure and acid fast staining for cryptosporidium and Isospora belli were applied in uncertain cases. Also in this study, occult blood was checked in stool specimens using Guaiac test based on peroxidase activity of haemoglobin colour change (Kumaravel et al., 2011).

Data Collection

In this study, the data of patients’ dossier were used with no intervention.

Data Analysis

After gathering the data including sex, parasite species, admission type and existence of blood in stool in each year, the data were analysed by SPSS 11.0 based on the study purposes. Ratio and rate for qualitative variables and mean and standard deviation for quantitative variables were used. To compare the qualitative variables, chi-square test was used and t-test was used to compare quantitative variables.

All patients’ data were absolutely confidential and the Helsinki statement was followed, and the study ethic was approved in the Research Committee of Department of Pathology, Tehran University of Medical Sciences.

RESULTS

In this study, a total of 124366 patients who visited Children’s Hospital Medical Central Laboratory underwent stool exam (during 18 years from 1991 to 2008).

Characteristics of the Study Population

In total 13 408 cases (10.78%) had parasitic infections and 110 958 cases (89.22%) did not have parasitic infections in their stool exam. In the present study, 75 299 cases (60.54%) were male and 49 067 cases (39.46%) were female.

Characteristics of the Parasite-positive Group

The prevalence of parasitic infections including protozoa and intestinal worms was 7998 cases (10.62%) in males and 5410 cases (11.02%) in female which shows higher prevalence of infection in female patients (Table 1); meanwhile, the difference in prevalence of parasitic infection between males and females was statistically significant (P = 0.025). Of them, 50.352% were pathogenic protozoa including Giardia lamblia, Cryptosporidium, Isospora belli and Entamoeba histolytica/dispar (Table 3).

Table 1. Distribution of intestinal parasites according to sex.

	Positive		Negative		Total
Sex	No.	Percentage	No.	Percentage	No.
Male	7998	10.62	67 301	89.38	75 299
Female	5410	11.02	43 657	88.98	49 067
Total	13 408	10.78	110 958	89.22	124 366

Table 3. Prevalence of parasitic infections with protozoan parasites from 124 366 cases.

Parasite	No. of positive	Percentage of positive
Giardia lamblia	6306	49.33
Blastocystis hominis	3986	31.18
Entamoeba coli	1760	3.76
Chilomastix mesnili	74	0.57
Endolimax nana	193	1.5
Trichomonas hominis	95	0.74
Entamoeba histolytica/dispar	194	0.74
Iodamoeba butschlii	137	1.07
Cryptosporidium	29	0.22
Isospora belli	8	0.062
Total	12 782	100

From the total number of subjects, 78 443 cases (63%) were hospitalized at children ward and 45 924 cases (27%) were outpatients. The prevalence of parasitic infection in hospitalized patient at children ward was 4470 cases (5.70%), while this prevalence was 8938 cases (19.46%) in outpatients (Table 2), which showed that the prevalence of the infection was significantly higher in outpatients (P<0.001).

Table 2. Distribution of intestinal parasites in outpatients and inpatients.

	Positive		Negative		Total
	No.	Percentage	No.	Percentage	No.
Inpatient	4470	5.7	73972	94.3	78442
Outpatient	8938	19.46	36986	80.54	45924
Total	13 408	10.78	110 958	89.22	124366

Parasitic infection of all positive cases was related to protozoa in 12 782 cases (95.33%) and intestinal worms in 624 cases (4.87%). The most parasitic infection was G. lamblia which allocated 43.93% of infections in protozoa group. Blastocystis hominis (31.18%) and Entamoeba coli (13.76%) were ranked in next stages. Table 3 shows the prevalence of parasitic infections with protozoan parasites. Among intestinal worms, the highest prevalence was related to Hymenolepis nana (40.7%), followed by Ascaris (24.2%) and Oxyure (21.2%) in the performed tests (Table 4).

Table 4. Prevalence of parasitic infections with intestinal worms from 13 408 cases of positive stool samples.

Parasite	No. of positive	Percentage of positive
Hymenolepis nana	255	40.7
Ascaris	152	24.2
Oxyure	133	21.2
Tenia saginata	32	5.1
Fasciola hepatica	7	1.1
Trichuris trichiura	11	1.7
Strongyloides stercoralis larvae	14	2.2
Dicrocoelium dendriticum	19	3.01
Hymenolepis diminuta	3	0.47
Total	626	100

Table 5. Comparison of the frequency of parasites between the first 10 years and next 8 years of the study.

	First 10 years	Next 8 years	P value
Positive cases for intestinal worms	571 (8%)	55 (1%)	<0.001
Positive cases for protozoas	10 461 (14.9%)	2321 (4.3%)	<0.001

Total number of test requests for occult blood was 43 457 in 18 years in which 1471 (3.28%) of the cases were positive. The most positive result was related to G. lamblia (46.97%) followed by B. hominis (31.95%) and E. histolytica/dispar.

In this study, comparison of the frequency of parasites between the first 10 years and next 8 years of the study has been carried out which revealed that from the total stool exams carried out in the first 10 years of study (70 112 cases), 571 cases were positive for intestinal worms (8%), but in the next 8 years (54 254 cases), there were just 55 positive cases of the intestinal worms (1%) that this difference was significant by chi-square test (P<0.001). In performed stool exam in the first 10 years of the study (70 112 cases), 10 461 cases were positive for protozoas (14.9%). but in next 8 years (54 254 cases), there were just 2321 positive cases for protozoas (4.3%) which revealed a significant difference (P>0.001) (Table 4).

DISCUSSION

In the present study, the overall prevalence was 10.78% with G. lamblia as the most common protozoa followed by B. hominis and E. coli and H. nana as the most common intestinal worm followed by Ascaris (24.2%) and Oxyure. In a study carried out by Morales–Espinoza et al. (2003) on children under 15 years old about the prevalence of intestinal parasitic infections, which collected stool specimens and examined them in 32 Mexican border area, the prevalence of parasitic infection was 67% in 1478 cases which was a large number. Also 60% was suffering from different parasitic infections(Morales–Espinoza et al., 2003). Anotherstudy carried out by Patel and Khandekar (2006) which determined the prevalence of parasitic infections in school children in Oman, stool specimens of 467 students between 9 and 10 years were assessed from 2004 to 2005 which revealed that the prevalence of these infections was 38% (Patel and Khandekar, 2006). The overall infection rate in another research carried out by Jamaiah and Rohela on total of 246 stool samples was 6.9% and Trichuris trichiura was the most common parasite (Jamaiah and Rohela, 2005). Winsberg et al. reported an overall intestinal parasite prevalence rate of 18.6% in Latino residents of Chicago with specific rates of Trichuris trichiura, hookworm Giardia lamblia and Strongyloides stercoralis in their work, although several non-pathogenic protozoa were found, there were no cases of Ascaris lumbricoides or Entamoeba histolytica (Winsberg et al., 1975). In a similar work performed by Eligail et al., most common infections were due to the non-pathogenic organisms such as E. coli, Iodamoeba buetschilii and Endolimax nana, but among the different pathogenic parasites, Ascaris and G. lamblia were found to be the most prevalent ones in their study (Eligail et al., 2010).

Magambo et al. in a study about the prevalence of intestinal parasites among children in southern Sudan found a prevalence of 13.1% for hook worms and they did not detected A. lumbricoides and cestodes in their study population (Magambo et al., 1998). The study carried out by Wani et al. in India showed that of the 514 students surveyed, 46.7% had one or more parasites in which the prevalence of A. lumbricoides was the highest (Wani et al., 2007). In a similar work, Okyay et al. reported 31.8% of parasitic infection with one or more intestinal parasites in school children in Turkey and they revealed E. vermicularis, G. intestinalis and E. coli as the three most common parasites (Okyay et al., 2004). Jacobsen et al.’s work on 293 children aged 12–60 months found E. histolytica to be the most prevalent infection followed by A. lumbricoides, E. coli and G. lamblia (Jacobsen et al., 2007).

Nematiyan et al. performed a study about the prevalence of intestinal parasitic infections on school children and relationship with patients’ socioeconomic level: 19 213 subjects participated in their study and 19 209 data were collected (>99.99% participation rate) which showed 18.4% infection and 2% co-infection of two or three parasites (Nematian et al., 2004).

In a study performed by Heidari and Rokni, there was one species of pathogen or non-pathogen parasites in at least 68.1 of children in day-care centres who were tested. They reported a significant difference between the rate of infection and parents’ education, but found no relationship between age, sex and health houses (Heidari, 2003). In this study, the prevalence of parasitic infection was higher in females, which was similar to that in the study of Massoud et al. (1980), which was significantly higher in females than in males, but there was no significant difference in age in other similar studies based on the literature review.

Higher prevalence of parasitic infection of outpatients in this study is in good agreement with the findings of the similar studies (Lopez–Brea and Vallejo, 1994), and the findings of this study about the characteristics of occult blood testing and the parasites associated with this feature correspond with the similar studies. In the study of Eligail et al. (2010), 5.56% of cases were found to be positive for occult blood and 19.44% of cases were slightly positive.

A comparison between the first 10 years and the next 8 years of the study showed that the prevalences of intestinal parasites were 8% and 1%, respectively (P<0.001) and the rates for protozoal infection were 14.9% and 4.3%, respectively (P<0.001), which means better level of sanitation in the life of residents. The prevalence of intestinal parasites was reduced during recent years (Table 5); however, more attempts should be carried out to make it lower.

CONCLUSION

Considering the high number of patients participating in this investigation, the present study can be a good reference in demonstrating the epidemiology and the pattern of intestinal parasites in children to that the suitable diagnostic test and treatments could be conducted for the affected patients.