FREQUENCY OF INTESTINAL PARASITIC INFECTIONS AMONG SCHOOLCHILDREN IN IBB CITY-YEMEN

Eglal Ahmed Qasem¹, Wadhah Hassan Edrees^2*, Wadee Abdullah Al-Shehari¹, 

Mohammed Ali Alshahethi³

¹Department of Microbiology, Faculty of Medical Sciences, Ibb University, Yemen

²Medical Laboratory Department, Faculty of Medical Sciences, Al-Razi University, Yemen

³Department of Biology, Faculty of Education and Arts, Amran University, Yemen

ABSTRACT  

Objectives:  Intestinal parasitic infections are widely distributed and remain one of the most health problems in Yemen. This is a cross-sectional study aimed to determine the prevalence of intestinal parasitic infection and associated factors among schoolchildren in Ibb City, Yemen. 

Methods:  A total of 300 stool samples were collected from schoolchildren between January to April 2018 and examined by direct smear and formalin ether concentration techniques.

Results:  The result showed that 62.7% were positive for intestinal parasites, with a higher frequency of single than multiple infections (85.1 vs. 14.36%, respectively). Also, 85.64% were infected by protozoa whereas 14.36% infected by helminths. The prevalence of infection was 61.70% for Entameba histolytica, 23.94% for Giardia lamblia, 7.45% for Ascaris lumbricoides, 4.3% for Hymenolepis nana, and 2.61% for Enterobius vermicularis. Moreover, the highest prevalence of E. histolytica, G. lamblia, and A. lumbricoides was within group aged 9-12 years. H. nana was between age groups of 9-12 and 13-16 years while E. vermicularis was found among 5-8 and 9-12 years. In addition, females were 69% infected significantly higher than males 54.55%. Besides, the various signs and symptoms associated with intestinal infections have been documented.

Conclusion:  High prevalence of intestinal infection was documented among schoolchildren drinking from cistern water, poor hygiene practices, poor food sanitation, non-swimming, and non-previously treated for Schistosoma parasite. High frequency of intestinal parasitic infection between schoolchildren in the study area requires more effort to implement the appropriate programmers that warrant to control and prevention the prevalence of intestinal parasitosis.

Keywords: Ibb City, intestinal parasitic, prevalence, schoolchildren, Yemen.

INTRODUCTION

Intestinal parasitic infection, caused by protozoa and helminths, is one of the world's largest health problems and is responsible for affecting nearly 3.5 billion people and about 450 million illnesses caused by intestinal parasites¹. The highest prevalence of parasitosisis concentrated in developing countries with up to 50%². Many factors play an important role in developing countries for transmission of the intestinal parasites the representing the unavailability of potable water, reduced hygienic environments, fast population growth, and, low economic status^3,4. Intestinal parasitic infections are the most threats that challenge the healthy living in developing countries mainly affecting school children⁵.

The young children are found to be too much affected within intestinal parasites compared to adults because of their increased requirements of nutrition and weak immune systems. The presence of intestinal parasites in this age group have been accompanied with significantly risk problems such as slowly in growth, lack of protein-energy malnutrition, iron deficiency, decrease in physical activity, and impaired mental function and learning ability⁶. It was estimated that around 12% of the world wide illness burdens resulting from intestinal parasites are reported amongst children aged 5-14 years old in developing countries⁷. Also, nearly 270 million pre-school and 600 million schoolchildren are living in a zone where the parasites are extensively transmitted⁸.

In developing countries, the intestinal parasites such as Entameba histolytica, Giardia lamblia, Enterobius vermicularis, and Hymenolepis nana are more easily spread and more frequently between children⁹. Yemen belongs to the developing countries that lack the strategies and programs for eradicating or preventing transmission the parasitic infection among the population. There are several reports have been performed to evaluate the infections of intestinal parasitic between children in Yemeni communities. A study by, in Hadramowat, Al-Haddad and Baswaid¹⁰ found that the most infective parasites prevailed in children were G. lamblia, E. histolytica, Ascaris lumbricoides, Trichuris trichiura, H. nana, Taenia saginata, and Schistosoma mansoni. However, in Sana’a, Alyousefi et al.,¹¹ reported that the intestinal parasites among children were G. duodenalis, E. histolytica/dispar, Cryptosporidium,  A. lumbricoides, S. mansoni, H. nana and E. vermiculari recorded in urban and rural areas. Also, it was reported that 75.4% of examined children under 12 years in Taiz districts were infected with E. histolytica/dispar, G. duodenalis, A. lumbricoides, H. nana, S. mansoni¹². Moreover, Alwabr and Al-Moayed¹³ recorded that the E. histolytica, S. mansoni, T. trichiura, and E. vermicularis were reported between schoolchildren in Al-Mahweet governorate. One study only was conducted in Ibbcity, in 2010, and showed E. histolytica, G. lamblia,  A. lumbricoides, T. trichiura, H. nana, S. mansoni, Ancylostoma duodenale, E. vermicularis, and Strongyloides stercoralis the most prevalent intestinal parasitic among children¹⁴. This study is small and not enough to show the occurrence of intestinal parasitic among schoolchildren and related factors. Therefore, the aim of the current work was to determine the prevalence of intestinal parasitic infections and risk factors for parasite infection among schoolchildren in Ibb, Yemen.

MATERIALS AND METHODS

Study Design and Area

A cross-sectional study was carried out at medical laboratory department, Ibb University which located in Ibb city, Yemen, during the period from January to April 2018. There were seven districts subjected for present workthat are Al-Dehar, Al-Maeen, Al-Mashanh, Al-Sabal, Harathah, Mafrg-Jeblah, and Shabanthat located in Ibb city. From each district, one school was selected randomly.

Ethical statement

The study protocol was permitted by the University of Ibb, Yemen, and authorization to start collection of data was granted by the Education Office of the City of Ibb. Before the start of data collection and samples, the goals and methods of study were explained to the school principals and children to agree to their inclusion in this study.

Data Collection

A designed questionnaire was subjected to each participant such as age, gender, the clinical information like diarrhea, blood in the stool, and abdominal pain as well as environmental factors like; source of drinking water, personal hygiene, food sanitation, parents occupation, swimming, and previous Schistosoma treatment. 

Sample Collection and Examination

A total of 300 stool samples were chosen of schoolchildren, aged between 6-16 years old, attending governmental schools. A dry, clean, leak proof container (labeled faecal) was given to each child and was instructed on how to introduce specimens (stool) into the bottles and transmitted to a laboratory, as soon as possible, for parasitological examination¹⁵. The specimens were prepared and tested by using three methods of routine examination of stool: wet preparation, saline sedimentation centrifuged, and formalin/ether concentration¹⁵.

Table 1: The distribution of collected specimens according to gender and age

RESULTS

Three hundred (300) specimens were chosen of school children presenting to seven governmental schools in Ibb city. Of these samples, 168(56%) were females and 132 (44%) were males. The distribution of collected samples according to age was listed in Table 1. The distribution of collected samples according to districts was figured in Figure 1. It was collected 48 (16%) samples from Al-Dehar, 43 (14.3%) samples from Al-Maeen, 39 (13%) samples from Al-Mashanh, 37(12.3%) samples from Al-Sabal, 44(14.67%) samples from Harathah, 47 (15.67%), and samples from Mafrg-Jeblah, and 42 (14%) samples from Shaban. Out of 300 schoolchildren samples, 188 (62.7%) were recorded positive for parasites infection while 112 (37.3%) samples were reported negative for parasitic infection as shown in Figure 2. Furthermore, multiple infections were obviously identi?ed and documented that 160(85.1%) of the positive samples were infected with one type of parasite species, while 28 (14.9%) were infected by double types of parasites (Table 2). 

Table 2: Multiplicity of parasitic infections among schoolchildren

Figure 3 shows that the 161 (85.64%) of the positive samples were infected by intestinal protozoa (cyst) while 27(14.36%) of the positive samples were infected by intestinal helminthes (eggs). The present results showed that the most predominate of intestinal parasites was E. histolytica with 116(61.70%) followed by G. lamblia 45(23.94%), A. lumbricoides 14 (7.45%), H. nana 8(4.3%), and E. vermicularis 5(2.61%) as listed in Table 3. The occurrence of intestinal parasitic infection according to age highest prevalence of E. histolytica was reported among the age group of 9-12 years (41.4%) followed by the age of13-16 years (37.9%). 

Table 3: Prevalence of intestinal parasites among schoolchildren

The high rate infections were 51.1% and 57.1% recorded between 9-12 years by G. lamblia and A. lumbricoides, respectively. Also, the similar results of H. nana infection were (50%) reported between groups aged 9-12 and 13-16 years while infection E. vermicularis infection was found among 5-8 years and 9-12 years as listed in Table 4.Moreover, the overall rates of intestinal parasitic infection were recorded 69.1% and 54.55%, respectively, in females and males Table 4. Table 5 summarizes the common signs and symptoms among infected schoolchildren. It was revealed that the high rate was 49.3% recorded with an abdominal pain followed by 46.7% for diarrhea. While the low rate was with 8% with bloody in the stool. The results based on factors were found that the frequency of intestinal parasitic infection among schoolchildren drinking from the cistern with 76.6%, poor hygiene with 76.1%, poor food sanitation with 57.4%, no swimming practice 68.1%, not previously treated for Schistosoma68.1%as listed in Table 6.

Figure 1: The collected samples according to districts 

DISCUSSION

Recently, the high rate of intestinal parasites prevalence among children in Yemen is well-known. The major factors associated with the incidence of intestinal parasitic diseases refer to the low hygienic practices, environment contamination with fecal, lack of safe water, and health education resulting from the high level of poverty¹³. The present study was revealed that 300 samples (168 females and 132 males) were collected from schoolchildren from Ibb city. 

Figure 2: Positive and negative for parasitic infection

It was observed that 62.7% of samples were reported positive for intestinal parasitic infection while 37.3% were reported negative. Similar studies reported from different regions of Yemen including Hadramowat governorate (58.7%)¹⁰, Ibb (57.4%)¹⁴, and Sana’a (54.8%)¹⁶. However, the low prevalence was reported in Yemen; in Taiz 38.2%¹², in Sana’a city 40.3%¹¹, while the higher prevalence was in Al-Mahweet governorate with 90%¹³. The current work showed that the multiple infections at 14.9% with two types of parasites. Similarity, the previous studies were reported the multiple infections in Yemen; in Sahar district 3%¹⁷, in Sana’a city 11.7%¹¹, and in Sana’a governorate 8.5%¹⁶, in Al-Mahweet 75.5%¹³. 

Figure 3: Type of intestinal infection among schoolchildren

In the current investigation, the intestinal protozoa were 85.64% the most predominant infections observed among schoolchildren, while the intestinal helminthes infections were (14.36%). A similar result was reported by Al-Mekhlafi et al.,¹⁶ found thatprotozoa and helminthic infections were 37.6% and 17.2%, respectively, recorded among rural schoolchildren in Sana’a. In this result showed that the E. histolytica was the most prevailed of intestinal parasitic infection with 116 (61.70%) followed by G. lamblia 45(23.94%), A. lumbricoides 14(7.45%), H. nana 8 (4.3%), and E. vermicularis 5(2.61%). This result is consistent with previous studies conducted in Yemen. A study by Alsubaie et al.,¹⁴ documented that the high prevalence of intestinal parasitic was E. histolytica (33.7%), G. lamblia (23.6%), A. lumbricoides (14.3%), T. trichiura (9.3%), H. nana (6.2%), S. mansoni (3.1%), A. duodenale (1.2%), E. vermicularis (0.8%), and S. stercoralis (0.8%). However, a study by Alwabr and Al-Moayed¹³  recorded that the most common intestinal parasites prevalence were E. histolytica (64%) followed by S. mansoni (36.5%), Trichuristrichiura (18%), and E. vermicularis (13%). Another study by AL-Harazi¹² reported that the 75.4% of examined children were infected with E. histolytica/dispar (20.6%), G. duodenalis (12.4%), A. lumbricoides (3%), H. nana (0.9%), and S. mansoni (0.9%) in an urban and rural area.

Table 4: Distribution of intestinal parasitic infections in relation to age and gender

In contrast, Alyousefi et al.,¹¹ observed that the frequency rates of intestinal parasites were G. duodenalis (17.7%) followed by E. histolytica/dispar (17.1%), A. lumbricoides (2.4%), H. nana (1.4%), E. vermicularis (0.4%), and S. mansoni (0.3%). Also, Al-Haddad and Baswaid¹⁰ found that the most parasites prevailed in children were G. lamblia (19.17%), E. histolytica (16.83%), A. lumbricoides (15.83%), T. trichiura (2.33%), H. nana (2.33%), T. saginata (1.50%), and S. mansoni (0.67%). E. histolytica and G. lamblia consider the most of prevalent protozoan parasite among children and cause of intestinal morbidity. E. histolytica infects annually about 500 million cases and causes around 50 million of amoebic dysentery and invasive amebiasis diseases and kills about 100 thousand persons^18,19. G. lamblia responsible for about 200 million cases every year²⁰. Also, A. lumbricoides and T. trichiura are responsible for about 1.2 billion and 795 million, respectively, infections globally²¹.

Table 5: Clinical signs and symptoms among infected schoolchildren

The prolonged of parasitosis diseases lead to bleeding of intestinal, mal-absorption and deficiency of nutrients, damage of cells and tissues. In eventually these results generally effect in retardation of growth, slow height-weight development, impaired in mental development, school absence, low academic performance, predisposed to malnutrition and infection^22,23. In current work, the highest prevalence of E. histolytica, G. lamblia, and A. lumbricoides infection was recorded on group aged 9-12 years. While the age groups of 9-12 and 13-16 years were 50% infected by H. nana. The E. vermicularis infection was found between 5-8 years and 9-12 years old. These results are in agreement with Alwabr and Al-Moayed¹³ who observed that the high prevalence of intestinal parasitic infection was (43%) recorded in the age group 10-12 years. This could be clarified by the extreme movement of children at this age and they may become more susceptibility to infected water while swimming/playing or fetching water for domestic purposes or helping in agriculture activities²⁴. In the present study, the prevalent intestinal parasites in females with 69% was significantly higher than males (54.55%).Conversely, the previous study by Alwabr and Al-Moayed¹³ reported that the infection rates between males (46.5%) were higher than females (43.5%). 

Table 6: Factors associated with intestinal parasitic infection among schoolchildren

The present result showed that the majority of clinical signs and symptoms sufferings are associated with the main parasites in Yemen such as E. histolytica and Giardia. Also, blood in the stool, cough, muscle aches, skin itch and weight loss were shared with all parasitic infections and another illness. This result was supported by Al-Haddad and Baswaid¹⁰ who found that different symptoms as diarrhea, abdominal pain, abdominal distention, constipation, nausea and vomiting, and fever were presented between participated. The effect of intestinal parasites on children weight was investigated in Yemen. Alwabr and Al-Moayed¹³ showed that more than 67% of the infected schoolchildren were found to be underweight and 22% stunting. High prevalence of intestinal infection in this work was recorded among schoolchildren drinking from cistern water, poor hygiene practices, poor food sanitation, non-swimming, and non-previously treated for Schistosoma parasite. The environmental and behavioral factors could be played a major role in prevailing of intestinal parasitic infections with high rate in the study area.

CONCLUSION

It can be concluded that the high frequency of protozoa and helminthes infections reported in the present investigation indicated poor hygiene and environmental pollution as a problem of public health among schoolchildren in the area. Therefore, there are more efforts to implement the appropriate programmers that warrant to control and prevention the prevalence of intestinal parasitosis among schoolchildren.

ACKNOWLEDGMENTS

The authors thank the teams work;Amal Al-Suhaily, Sarah Al-Sadi, Lina Al-Kamel, ShimaObid, Sana Alsorabi, Kefah Al-Morady, Heba Al ahmadi, Sawsan Al-Ahmadi, Halah Hasan for participating in this work.

AUTHOR’S CONTRIBUTION

The manuscript was carried out, written, and approved in collaboration with all authors.

CONFLICT OF INTEREST  

No conflict of interest associated with this work.

REFERENCES

1. Okyay P, Ertug S, Gultekin B, Onen O, Beser E. Intestinal parasites prevalence and related factors in school children, a western city sample-Turkey. BMC Public Health 2004:4(64).

2. Chacon-Cruz E, Mitchell D. Intestinal protozoal diseases. Medicine J 2003; 3(5):1–11.

 https://doi.org/10.1186/1471-2458-4-64

3. Sayyari AA, Imanzadeh F, et al. Prevalence of intestinal parasitic infections in the Islamic Republic of Iran. Eastern Mediterranean Health J 2005; 11(3): 377-383.

4. Mohammed K, Abdullah M, Omar J. Intestinal parasitic infection and assessment of risk factors in North-western. Nigeria: a community based study. Int J Pharm Med Bio Sci 2015; 4(2):141–145.

https://doi.org/10.18178/ijpmbs.4.2.141-145 

5. Kia EB, Hossein M, et al. Study of intestinal protozoan parasites in rural inhabitants of Mazandaran province, northern Iran. Iranian J Parasitol 2008; 3:22–25.

6. Sackev M-E. Intestinal factors and parasite infections: prevalence, risk factors and consequences for child growth, Iron status and development in rural Ecuador. Msc. Thesis; Virginia Polytechnic and State University; Ecuador; 2001.

7. Awasthi S, Bundy D, Savioli L. Helminthic infections. British Med J 2003; 323:431-433.

8. World Health Organization. Soil-transmitted helminth infections. Geneva: WHO; 2016.

9. World Health Organization. Soil-transmitted helminthiases. In: Eliminating soil-transmitted helminthiases as a public health problem in children: Progress report 2001–2010 and strategic plan 2011–2020. WHO, Geneva. 2012; 18-85.

10. Al-Haddad A, Baswaid S. Frequency of intestinal parasitic infection among children in Hadhramoutgovernorate (Yemen). J Egypt Soc Parasitol 2010; 40: 479-486.

11. Alyousefi NA, Mahdy MK, Mahmud R, Lim YL. Factors associated with high prevalence of intestinal protozoan infections among patients in Sana’a City, Yemen. PLoS ONE. 2011; 6(7): e22044. 

 https://doi.org/10.1371/journal.pone.0022044

12. AL-Harazi T. Prevalence and risk factors associated with intestinal parasitic infection among patients in Taiz City, Yemen. British Micro Res J 2016; 16(3): 1-7. 

https://doi.org/10.9734/BMRJ/2016/28317

13. Alwabr AG, Al-Moayed E. Prevalence of intestinal parasitic infections among school children of Al-Mahweet Governorate, Yemen. Eur J Biol R  2016; 6(2): 64-73.

14. Alsubaie AR, Azazy AA, Omer EO, Al-Shibani LA, Al-Mekhlafi AQ, Al-Khawlani FA. Pattern of parasitic infections as public health problem among school children: A comparative study between rural and urban areas. J Taibah Univ Med Sci 2016; 11(1):13–18.

http://dx.doi.org/10.1016/j.jtumed.2015.10.006

15. Cheesbrough M. District laboratory practice in tropical countries. Part 1, 2^nd ed. Cambridge, 2010; 200-208.

16. Al-Mekhlafi AM, Abdul-Ghani R, Al-Eryani SM, Saif-Ali R, Mahdy MA. School-based prevalence of intestinal parasitic infections and associated risk factors in rural communities of Sana'a, Yemen. Acta Trop 2016; 163: 135-141.http://dx.doi.org/10.1016/j.apjtm.2017.09.011

17. Raja’a YA, Mubarak JS. Intestinal parasitosis and nutritional status in school children of Sahar district, Yemen. Eastern Mediterranean Health J 2006; 12: 189-194.

18. Baxt LA, Singh U. New insights into Entamoeba histolytica pathogenesis. Curr Opin Infect Dis 2008; 21: 489–494.

https://doi.org/10.1097/QCO.0b013e32830ce75f

19. World Health Organization. Entamoeba taxonomy. Bull. World Health Organ.1997; 75: 291–294.

20. Feng Y, Xiao L. Zoonotic potential and molecular epidemiology of Giardia species and giardiasis. Clin Microbiol Rev 2011; 24: 110–140.

https://doi.org/10.1128/CMR.00033-10

21. Alum A, Rubino J, Ljaz M. The global war against intestinal parasites -should we use a holistic approach? Int J Infect Dis 2010; 14:732–738.

22. BrookerS. Estimating the global distribution and disease burden of intestinal nematode infections: adding up the numbers: A review. Int J Parasito 2010; 40(10):1137–1144.

https://doi.org/10.1016/j.ijpara.2010.04.004

23. Shamsan ENA, De-ping CAO, Al-Shamahy HA, Al-Hajj MA, Bo-fan J, Yaogang Z. Coccidian intestinal parasites among children in Al-Torbah city in Yemen: in country with high incidence of malnutrition. Univ J Pharm Res 2019; 4(4): 25-29. 

https://doi.org/10.22270/ujpr.v4i4.301

24. Sady H, Al-Mekhlafi HM, Mahdy MAK, Lim YAL, Mahmud R, Surin J. Prevalence and associated factors of schistosomiasis among children in Yemen: implications for an effective control programme. PLoSNegl Trop Dis 2013; 7(8): e2377. https://doi.org/10.1371/journal.pntd.0002377