Frequency of Intestinal Parasitic Infection Among Working Children in Tehran, Iran

authors:

avatar Borna Salemi 1 , avatar Abdoulreza Esteghamati ORCID 2 , avatar Shirin Sayyahfar 2 , avatar Farah Bokharaei-Salim ORCID 3 , avatar Hossein Keyvani ORCID 3 , avatar Khadijeh Khanaliha ORCID 2 , *

Student Research Committee, School of Medicine, Iran University of Medical Sciences, Tehran, Iran
Research Center of Pediatric Infectious Diseases, Institute of Immunology and Infectious Diseases, Iran University of Medical Sciences, Tehran, Iran
Department of Virology, School of Medicine, Iran University of Medical Sciences, Tehran, Iran

how to cite: Salemi B , Esteghamati A, Sayyahfar S, Bokharaei-Salim F, Keyvani H, et al. Frequency of Intestinal Parasitic Infection Among Working Children in Tehran, Iran. Arch Pediatr Infect Dis. 2019;7(4):e93760. https://doi.org/10.5812/pedinfect.93760.

Abstract

Background:

Parasites infection is one of the public health issues among children all over the world. The limited available data indicates that working children often suffer from poor health.

Objectives:

In this study, the frequency of intestinal parasitic infection in working children related to Sobh-e Rooyesh School was evaluated for the first time in Tehran, Iran.

Methods:

Fresh stool samples were collected from 175 working children associated with Sobh-e Rooyesh School in Tehran and transferred to Research Center of Pediatric Infectious Diseases, Institute of Immunology and Infectious Diseases, Iran University of Medical Sciences, which then examined by the wet mount examination with Phosphate-buffered saline and formalin ether concentration and agar plate culture. The trichrome staining was performed using stool samples conserved in Phosphate-buffered saline.

Results:

The results showed that in general the frequency of parasitic infection was 77/175 (44%). The frequency of Blastocystis hominis as the most common parasites was (32.6%) followed by (9.1%) related to Giardia lamblia and (8%) samples were positive for Entamoeba coli. Frequency of helminthic infection was 3/175 (1.7%) including 2/175 (1.1%) Hymenolepis nana and 1/175 (0.57%) Ascaris lumbricoides.

Conclusions:

The frequency of intestinal parasitic infections was relatively high among working children in Tehran. Frequency of protozoan infection was more than that of helminth infection. It is suggested that additionally necessary treatment, health education and personal hygiene should be provided to prevent transmission.

1. Background

Parasitic infection is widely considered especially in children in developing countries due to poor health and low level of sanitation (1). The most common intestinal parasites such as Giardia lamblia (G. lamblia) and Blastocystis hominis (B. hominis) have been reported from several studies (2). The protozoan parasite, G. lamblia, causes gastroenteritis which is transmitted by water and the parasite is highly infective by ingestion of as few as 10 cysts in human (3, 4).

Soil-transmitted helminthes infections are distributed throughout the tropics and subtropics. Necator americanus (N. americanus), Ancylostoma duodenale (A. duodenale), Ascaris lumbricoides (A. lumbricoides) and Trichuris trichiura (T. trichiura) were reported from all over the world (5). The most prevalent helminth infection was Hymenolepis nana (H. nana), followed by A. lumbricoides and Enterobius vermicularis (E. vermicularis) from some previous studies (2).

High risk behavior and public health problems were found more greatly in persistent street children who live in street than those living in orphanage and resident institutes. They have poor health and limited access to health services, and they are considered as reservoir for parasitic diseases because of poor personal and environmental hygiene (6, 7), so global standards are necessary for legalization of working children rather than its condemnation (8). It is estimated that there are 100 million street children living over the world, however, real population is uncertain. It is thought that there are 40 million in Latin America alone (9).

There is some information about situation of parasitic infection in street children and working children in other countries (10, 11), but there was no data on the frequency of parasitic infection among working children in Iran.

2. Objectives

The aim of this study is to evaluate the frequency of intestinal parasitic infection in working children related to Sobh-e Rooyesh School in Tehran, Iran.

3. Methods

3.1. Sampling

This cross-sectional study was carried out between February and December, 2018. Fresh stool samples were collected from 175 working children associated with Sobh-e Rooyesh School in Tehran. The children’s ages were between 7 - 15 years, with the mean age of 9.5 years.

The Sobh-e Rooyesh is a school for working children in Tehran, Iran. It is the first school for working children in Iran. It was established in 2014 for children who have to work to earn money for their families. The school-aged children are educating at different grades at school. The school population was 341 including 187 boys and 154 girls in age group of 7 - 15 years in 2018 and the school located in at Harandi neighborhood, downtown Tehran. The students are educating in different grades and teaching different social skills and proper profession according to their talents and situation in order to choose jobs with good and healthy income instead of false and risky jobs in the future. All of children participated in this study back to residency or their relatives at night. The most of children live in their residency and some of them live with their father and mother.

Sampling was carried out by accidental method according to the formula which is calculated as n = Z2 × P (1 - P)/d2, where P is the prevalence of intestinal parasite in Tehran, d is 0.045 marginal error, and standard score (Z) is 95% confidence interval. The prevalence of intestinal parasites has been reported among a certain population in Tehran in previous study (12). The sample size was calculated at 172 and finally the sample size used in the study was 175.

The inclusion criteria was children associated with Sobh-e Rooyesh school and work as working children and were in age group of 7 - 15 years.

A questioner was filled up with the pieces of information about gender, age, education, nationality, life style, washing hands before eating meal or after taking toilet, contact with soil and animal.

3.2. Stool Examination

Fresh stool samples were collected from 175 working children associated with Sobh-e Rooyesh School in Tehran and transferred to Research Center of Pediatric Infectious Diseases, Institute of Immunology and Infectious Diseases, Iran University of Medical Sciences and then examined by wet mount examination with Phosphate-buffered saline (PBS) and formalin ether concentration and agar plate culture. A direct examination was performed on watery samples for diagnosis of trophozoites of protozoa and standard formalin-ether concentration method was used to conduct the examination under microscope with 100x and 400x as final magnification by an expertise technologist.

The trichrome staining was performed using stool samples conserved in PBS according to the method which was described previously (2). The permanent trichrome staining was performed for some suspected cases. The smears were prepared and after methanol fixation, smears were stained by the modified Ziehl-Neelsen technique to identify coccidia.

3.3. Analysis

The analysis was done using SPSS version 18 (Chicago, IL, USA) and chi-square, Predictive values test were used to analyze statistical relationship.

4. Results

In this study, 175 working children associated with Sobh-e Rooyesh School in Tehran were evaluated in order to trace parasitic infection and the results were as follows: 90 (51.4%) out of 175 were female and 85 (48.6%) were male. Most of the working children (144) were Afghan refugees and just 31 of them were Iranian. All children are studying in this school and working as street vendors or seamstress and porter and also clean vehicles.

The results showed that in total, the frequency of parasitic infection was 77/175 (44%) that 76/175 (43.4%) was related to protozoa infection including: 57out of 175 (32.6%) parasites were positive for B. hominis as the most common parasites and then 16 out of 175 (9.1%) samples were positive for G. lamblia followed by 14 out of 175 (8%) samples which were positive for Entamoeba coli (E. coli). The frequency of Chilomastix mesnili (C. mesnili), Dientamoeba fragilis (D. fragilis), and Iodamoeba butschilli (I. butschilli) were 4/175 (2.3%), 1/175 (0.57%), and 1/175 (0.57%) respectively. In general, the frequency of helminthic infection was 3/175 (1.7%) including 2/175 (1.1%) H. nana and 1/175 (0.57%) A. lumbricoides.

In this study, five children among 31 Iranian populations were infected with B. hominis including 3/31 children who were infected with B. hominis and 2/31 children were infected with B. hominis and G. lamblia as a mix infection.

In this study, 77 cases were infected with intestinal parasitic infection, which 57 (74%) was single infection, 18 (23.4%) parasitic infection was double infection and 2 (2.6%) was triple infection. The most prevalent double infection 9 (11.7%) associated with B. hominis and E.coli followed by B. hominis and G. lamblia 5 (6.5%), B. hominis and H. nana 2 (2.6%), B. hominis and D. fragilis 1 (1.3%) and B. hominis and C. mesnili 1 (1.3%). The triple infection was between B. hominis and E. coli and G. lamblia 1 (1.3%), B. hominis and E. coli and I. butschilli 1 (1.3%).

The association between risk factors and parasitic infection among 175 working children was summarized in Table 1. There was no statistically signification between gender, age, and infection in this study. The most parasitic infection was found in 7 - 9 aged children; however, there was no significant correlation between age and the parasitic infection. Among all the factors, only unwashed hands before eating with soaps or after using toilet are statistically associated with parasitic infection rate (P = 0.004).

Table 1.

The Association Between Risk Factors and Parasitic Infection Among 175 Working Children in Tehran, Irana

Risk FactorSamplePositiveNegativeP Value
Age, y0.16
< 107838 (48.7)40 (51.3)
≥ 109739 (40.2)58 (59.8)
Gender0.28
Male8535 (41.1)50 (58.8)
Female9042 (46.6)48 (53.3)
Eating with unwashed hands0.004*
Yes9953 (53.5)46 (46.5)
No7624 (31.6)52 (68.4)
Contact with animal0.30
Yes7330 (41.1)43 (58.9)
No10247 (46.1)55 (53.9)
Contact with soil0.22
Yes9143 (47.3)48 (52.7)
No8434 (40.5)50 (59.5)
Total1757798

5. Discussion

Parasites infection is one of the public health issues in children all over the world, but no data is available about parasitic infection in working children in Iran. In this study, parasitic infection was considered among working children in Iran for the first time.

The most common protozoan parasites were B. hominis and G. lamblia and then followed by E. coli among working children in present study. The most common three intestinal protozoa have been reported B. hominis, G. lamblia, and E. coli in children in some previous studies (10, 11).

Intestinal parasitic infection was evaluated among street children who lived in orphanages in Peru. The prevalence of pathogenic and non-pathogenic intestinal parasites was reported (66.3%) that the prevalence of pathogenic ones was (30.6%). The most prevalent nonpathogenic protozoa was E. coli (41.9%) and most pathogenic ones was G. lamblia (17.1%).Helminthes infection were as follow, H. nana (7.8%), T. trichiura (4.7%), A. lumbricoides (3.5%), Ancylostoma/Necator (1.2%) (10).

The rate of intestinal parasitic infection among street children in Metro Manila, Philippines was (62.0%) for one or more intestinal parasites. The most common protozoans were B. hominis (40.7%) then G. lamblia (11.6%) followed by E. histolytica (2.9%). The most prevalent helminthes infection was related to T. trichiura (44.8%) then A. lumbricoides (36%) and Hookworm (7%) (11).

The prevalence of parasitic infection in street children in Addis Ababa, Ethiopia was (71.8%). The most common helminthes infection was related to A. lumbricoides (34.9%) followed by T. trichiura (22.8%) and Taenia species (17.5%) and those related to protozoan were G. lamblia (9.6%) and E. histolytica/dispar (8.2%) (13).

As it is obvious, high rate of protozoan infection among street working children in different countries was found and the most common protozoans were B. hominis and E. coli and G. lamblia (10, 11, 13).These findings are in convenient with the result of protozoans infection in the present study; however, high rate of helminthes infection like A. lumbricoides, T. trichiura, Taenia species and H. nana were found among street working children in other studies in comparison with the present study with low rate of helminthes infection like H. nana and A. lumbricoides.

In a study which was conducted by Lander et al. parasitic infection rate was reported in (29.2%) of children in Brazil. The most common parasites was G. lamblia (12.9%) and the infection rate of E. histolytica/dispar was (3.7%), and frequency of Cryptosporidium sp was (1%).The most prevalent helminthic infection were related to T. trichiura (12%) and A. lumbricoides (10.5%) and the prevalence of H. nana was (0.3%).Double infection was reported in (9.2%) and triple infection in (2.5%) of children (14).

In a study, (74.7%) of the Tanzanian children were infected with at least one intestinal protozoa species. The infection rates of G. lamblia (16.4%), B. hominis (28.0%), E. coli (51.5%) and E. histolytica/E. dispar (18.0%) were observed in the children (15).

Recent reports in Iran have shown the prevalence of intestinal parasites in the general population to be between (18.4%) and (33.3%) (2, 16, 17), which high level of infection is attributed with protozoan infection. In comparison with protozoan infection, helminthes infection rate is relatively low, about 0% - 3.6%, in some previous studies (17).

At present, the incidence of helminthic infection in Iran has decreased unlike the past when helminthic infection was very common. Recent studies demonstrated the prevalence of ascariasis and strongyloidiasis are between 0.1% and 0.3% and the prevalence of hookworm is almost < 1% in Iranian population; however Hymenolepis and Enterobius infection are more common in Iran (18). The ruminants were found to be infected with hydatid cyst, fasciolosis, and dicrocoeliasis in different parts of Iran (19), so control of fasciolosis and echinococcosis need more consideration like the treatment of livestock and dogs (18).

According to the findings of the present study, the frequency of helminthic infection was (1.7%) including (1.1%) H. nana and (0.57%) A. lumbricoides. The results are compatible with other studies in Iran, with high level of protozoa infection and low level of helminthes infection.

The prevalence of infection for protozoa and helminthes infections in general population in Jiroft, Iran was (27.4%) and (1.8%), respectively. The most prevalent protozoans were B. hominis (13.7%) and G. lamblia (7.8%), and that of helminth was H. nana (1.1%).There was no significant correlation between gender and infection rate (2).

In the present study, coinfection was found from two to three parasites. The most common co-infection was identified between B.hominis and E. coli. This is compatible with result of pervious study that the most common co-infection has been reported between B. hominis and E. coli (2).

The parasitic infection rates in males and females were 35 (41.1%) and 42 (46.6%) respectively in the present study. There was no statistically signification between gender and infection. The result of some previous studies suggested that gender is not an important factor in intestinal parasitic infection (2, 17). Among risk factors, unwashed hands before eating with soaps or before using toilet are statistically associated with parasitic infection (P = 0.004); however there was no statistically signification between contact with soil and animal and parasitic infection in the present study and the result of this study confirmed that soil-transmitted helminthes were not common in the present survey. It seems person-to-person transmission is an important way to be infected in working children and contaminated food is supposed as another transmission route.

Parasitic infection among children was 25.1% in Bushehr, including B. hominis (7.4%), G. lamblia (5.9%), and E. coli (3.4%).The highest prevalence was found in children at education levels 4 and 5. The prevalence intestinal parasites was slightly higher among the girls 14.8% than the boys 10.3%, but difference was not significant (20).

In general, parasitic infection in schoolchildren Sari, Iran has been reported (33.3%).The most common parasites was B. hominis (13.5%) followed by G. lamblia (10.6%), E. coli (7.2%), Endolimax nana (1.5%). The most helminthic infection related to E. vermicularis (2.2%), Trichostrongylus sp. (2.1%) and Strongyloides stercoralis (1.6%) respectively. Although hand washing before eating was significantly associated with intestinal parasitic infection, there was no association between contact with soil and infection (17).

In general, in the present study, the frequency of protozoan infection was (43.4%) and that of helminth infection was (1.7%) among working children in Tehran. In this group of children due to life style and less sanitation condition, the rate of protozoan infection like B. hominis and then G. lamblia and E. coli are high in comparison with other children in different areas in Iran. The helminthic infection related to H. nana and A. lumbricoides is relatively low. In overall, due to limitation of the present study multicenter studies on working children and street children with large sample size are needed to evaluate parasitic infection in different areas in Iran in the future.

5.1. Conclusions

The frequency of intestinal parasitic infections was relatively high among working children in the present study. In comparison with protozoan infection, helminthes infection rate is relatively low. Training course to improve the level of hygiene and necessary treatment is suggested to prevent transmission.

Acknowledgements

References

  • 1.

    Shobha M, Bithika D, Bhavesh S. The prevalence of intestinal parasitic infections in the urban slums of a city in Western India. J Infect Public Health. 2013;6(2):142-9. [PubMed ID: 23537828]. https://doi.org/10.1016/j.jiph.2012.11.004.

  • 2.

    Barkhori Mahni M, Rezaeian M, Kia EB, Raeisi A, Khanaliha K, Tarighi F, et al. Prevalence of intestinal parasitic infections in Jiroft, Kerman Province, Iran. Iran J Parasitol. 2016;11(2):232-8. [PubMed ID: 28096858]. [PubMed Central ID: PMC5236101].

  • 3.

    Caccio SM, De Giacomo M, Aulicino FA, Pozio E. Giardia cysts in wastewater treatment plants in Italy. Appl Environ Microbiol. 2003;69(6):3393-8. [PubMed ID: 12788741]. [PubMed Central ID: PMC161540]. https://doi.org/10.1128/aem.69.6.3393-3398.2003.

  • 4.

    Hatam-Nahavandi K, Mohebali M, Mahvi AH, Keshavarz H, Khanaliha K, Tarighi F, et al. Evaluation of Cryptosporidium oocyst and Giardia cyst removal efficiency from urban and slaughterhouse wastewater treatment plants and assessment of cyst viability in wastewater effluent samples from Tehran, Iran. J Water Reuse Desalin. 2015;5(3):372-90. https://doi.org/10.2166/wrd.2015.108.

  • 5.

    Hotez PJ, Fenwick A, Savioli L, Molyneux DH. Rescuing the bottom billion through control of neglected tropical diseases. Lancet. 2009;373(9674):1570-5. [PubMed ID: 19410718]. https://doi.org/10.1016/S0140-6736(09)60233-6.

  • 6.

    Huang CC, Barreda P, Mendoza V, Guzman L, Gilbert P. A comparative analysis of abandoned street children and formerly abandoned street children in La Paz, Bolivia. Arch Dis Child. 2004;89(9):821-6. [PubMed ID: 15321856]. [PubMed Central ID: PMC1763218]. https://doi.org/10.1136/adc.2003.042911.

  • 7.

    Woan J, Lin J, Auerswald C. The health status of street children and youth in low- and middle-income countries: A systematic review of the literature. J Adolesc Health. 2013;53(3):314-21 e12. [PubMed ID: 23706729]. https://doi.org/10.1016/j.jadohealth.2013.03.013.

  • 8.

    Wyness M. Global standards and deficit childhoods: The contested meaning of children's participation. Child Geogr. 2013;11(3):340-53. https://doi.org/10.1080/14733285.2013.812280.

  • 9.

    Abdullah MA, Basharat Z, Lodhi O, Wazir MH, Khan HT, Sattar NY, et al. A qualitative exploration of Pakistan's street children, as a consequence of the poverty-disease cycle. Infect Dis Poverty. 2014;3(1):11. [PubMed ID: 24661542]. [PubMed Central ID: PMC4022352]. https://doi.org/10.1186/2049-9957-3-11.

  • 10.

    Bailey C, Lopez S, Camero A, Taiquiri C, Arhuay Y, Moore DA. Factors associated with parasitic infection amongst street children in orphanages across Lima, Peru. Pathog Glob Health. 2013;107(2):52-7. [PubMed ID: 23683330]. [PubMed Central ID: PMC4001478]. https://doi.org/10.1179/2047773213Y.0000000073.

  • 11.

    Baldo ET, Belizario VY, De Leon WU, Kong HH, Chung DI. Infection status of intestinal parasites in children living in residential institutions in Metro Manila, the Philippines. Korean J Parasitol. 2004;42(2):67-70. [PubMed ID: 15181346]. [PubMed Central ID: PMC2717344]. https://doi.org/10.3347/kjp.2004.42.2.67.

  • 12.

    Arani AS, Alaghehbandan R, Akhlaghi L, Shahi M, Lari AR. Prevalence of intestinal parasites in a population in south of Tehran, Iran. Rev Inst Med Trop Sao Paulo. 2008;50(3):145-9. [PubMed ID: 18604414]. https://doi.org/10.1590/s0036-46652008000300003.

  • 13.

    Mekonnen B, Erko B, Legesse M. Prevalence of intestinal parasitic infections and related risk factors among street dwellers in Addis Ababa, Ethiopia. J Trop Dis. 2014;2(2). https://doi.org/10.4172/2329-891x.1000132.

  • 14.

    Lander RL, Lander AG, Houghton L, Williams SM, Costa-Ribeiro H, Barreto DL, et al. Factors influencing growth and intestinal parasitic infections in preschoolers attending philanthropic daycare centers in Salvador, Northeast Region of Brazil. Cad Saude Publica. 2012;28(11):2177-88. [PubMed ID: 23147959]. https://doi.org/10.1590/s0102-311x2012001100017.

  • 15.

    Speich B, Marti H, Ame SM, Ali SM, Bogoch ,I, Utzinger J, et al. Prevalence of intestinal protozoa infection among school-aged children on Pemba Island, Tanzania, and effect of single-dose albendazole, nitazoxanide and albendazole-nitazoxanide. Parasit Vectors. 2013;6:3. [PubMed ID: 23289920]. [PubMed Central ID: PMC3558385]. https://doi.org/10.1186/1756-3305-6-3.

  • 16.

    Haghighi A, Khorashad AS, Nazemalhosseini Mojarad E, Kazemi B, Rostami Nejad M, Rasti S. Frequency of enteric protozoan parasites among patients with gastrointestinal complaints in medical centers of Zahedan, Iran. Trans R Soc Trop Med Hyg. 2009;103(5):452-4. [PubMed ID: 19084249]. https://doi.org/10.1016/j.trstmh.2008.11.004.

  • 17.

    Daryani A, Sharif M, Nasrolahei M, Khalilian A, Mohammadi A, Barzegar G. Epidemiological survey of the prevalence of intestinal parasites among schoolchildren in Sari, northern Iran. Trans R Soc Trop Med Hyg. 2012;106(8):455-9. [PubMed ID: 22703897]. https://doi.org/10.1016/j.trstmh.2012.05.010.

  • 18.

    Rokni MB. The present status of human helminthic diseases in Iran. Ann Trop Med Parasitol. 2008;102(4):283-95. [PubMed ID: 18510809]. https://doi.org/10.1179/136485908X300805.

  • 19.

    Mohamadzadeh T, Shams S, Khanaliha K, Marhamatizadeh MH, Vafa A. A study on prevalence of some helminthic infections of the liver and lungs among ruminants in abattoir of Fars province, Iran. Arch Razi Inst. 2016;71(4):245-51.

  • 20.

    Barazesh A, Fouladvand M, Tahmasebi R, Heydari A, Kooshesh F. Prevalence of intestinal parasitic infections among primary school children in Bushehr, Iran. Avicenna J Clin Microbiol Infect. 2016;4(1). https://doi.org/10.17795/ajcmi-34335.