PREVALENCE OF INTESTINAL PROTOZOA, HELMINTHES, AND COCCIDIAN INFECTIONS AMONG PRIMARY SCHOOL CHILDREN IN THALA’A DISTRICT AT AMRAN GOVERNORATE, YEMEN 

Abdulsalam M. AL-Mekhlafi1image, Khaled Abdulkareem Al-Moyed2image, Hassan Abdulwahab Al-Shamahy2,3image, Ahmed Mohamed Al-Haddad4image, Azhar Azher Mohammed Al-Ankoshy5image, 

Emad Hassan Al-Shamahi2image 

1Department of Medical parasitology, Faculty of Medicine and Health Sciences, Sana’a University, Republic of Yemen.

2Medical Microbiology and Clinical Immunology Department, Faculty of Medicine and Health Sciences, Sana’a University.

3Medical Microbiology department, Faculty of Medicine, Genius University for Sciences &  Technology, Dhamar city.

4Department of Medical Microbiology, Faculty of Medicine and Health Sciences, Hadhramout University, Republic of Yemen.

5Physiology Department, Jabir Ibn Hayyan Medical University, Faculty of Medicine, Iraq.

ABSTRACT 

Background and objectives:  The prevalence of intestinal parasite infection, which can range between 18% and 90%, is one of the most frequently reported diseases in Yemen and poses a serious health issue for schoolchildren. In Thala’a District, Amran Governorate, Yemen, the study's main goal was to ascertain the prevalence of intestinal parasite infection among primary school students.

Subjects and methods: A cross-sectional survey was conducted from January to April 2022 among 400 schoolchildren, in the age groups 7-12 years. All the children were residents of the city of Thala’a. A pre-tested structured questionnaire was used to collect data. Stool samples were examined for intestinal parasites according to standard laboratory methods.

Results: The children's ages ranged from 7 to 12 years, with a mean±SD of 9.52±2.9 years. The results showed that 136/400 (34%) of the tested children were positive for intestinal parasite infection with a higher prevalence of specific intestinal worms (50.4%) than protozoa (33.3%) and coccidian infection (16.3%). The rate of infection alone was also higher than that of multiple parasitic infections (19.3% vs. 14.8%). The highest number of intestinal parasites was 50/400 (12.5%) for Ascaris lumbricoides, and 49/400 (12.25%) for Entameba histolytica followed by 9.8% for Giardia lamblia, 11.5% for Entrobius vermicularis, 6.5% for Cryptosporidium species, 6.5% for Hymenolepis nana, 2% for Schistosoma mansoni, and 0.8% for Trichuris trichiura. Considering the associated factors, boys had a higher infection rate than girls (50% vs. 24.2%) with an OR of 2.6, CI =1.7–3.9 (p < 0.001). A higher rate was also recorded in older children (41%) with an odds ratio of 1.6 (p=0.03).

Conclusion: There is a high prevalence of intestinal parasites among school children in Thala’a city, and various control measures are required to control and prevent intestinal parasites among school children.

Keywords:  Intestinal parasitic infections, prevalence, schoolchildren, Thala’a district, Yemen.

 

INTRODUCTION

 

One of the world's major health issues is the intestinal parasitic diseases, which can be brought on by both the protozoa and helminthes parasites. These infections can affect up to 3.5 billion people worldwide, with 450 million of those cases being directly attributable to intestinal parasites1. According to estimates of up to 50%, parasite infection is highly prevalent in impoverished nations2-5. In developing nations, a number of conditions, including a lack of drinkable water, poor environmental hygiene, rapid population increase, and low economic status, have a significant influence in the transmission of intestinal parasites6,7. Intestinal parasite infection poses the greatest risk to the children in underprivileged areas.

The poor development of the immune system and high susceptibility of youngsters to serious infection caused by their increasing nutritional needs. They are more likely to suffer from negative consequences such stunted growth, decreased physical activity, impaired cognitive function, and poor learning ability8,9. According to estimates, children between the ages of 5 and 14 in underdeveloped nations account for roughly 12% of the world's illness burdens brought on by intestinal parasites10. Additionally, according to the World Health Organization (WHO)11, as many as 270 million and 600 million preschoolers and schoolchildren, respectively, reside in regions with widespread parasite transmission. Entameba histolytica, Giardia lamblia, Hymenolepis nana, and Enterobius vermicularis are among the intestinal parasites that are disseminated more readily and more frequently among children in underdeveloped nations12. Coccidian is an essential microscopic parasite that infects the intestinal tract of most human and animal organisms. These organisms are a major concern for the clinicians, especially with the increasing rate of HIV infection and immuno-compromised cases. Coccidian parasites (Cryptosporidium spp., Isospora belli, and Cyclospora spp.) are the most common intestinal parasites in immunocompromised patients that can usually lead to fatal acute diarrhea while causing mild and limited gastrointestinal disturbances in individuals with a normal immune system13-16. The above-mentioned variables contribute to the underestimating of the significance of this illness because it is consistently viewed as a parasite that is neglected and there aren't enough investigations, particularly in Yemen17. Globally and in Yemen, a number of risk factors for coccidian parasites have been documented, including the use of tainted drinking water, contact with animals, a lack of sanitation, and poverty. Children are also at risk for contracting this infection18. Yemen is a developing country that lacks programming strategies to eliminate or control the transmission of parasitic infections in the population. The prevalence of intestinal parasitic infection among children in different regions of Yemen has been recorded in several reports and at a high rate3-5, 19. Also in Yemen, the spread of coccidian parasites has not been studied, among immunocompromised patients as well as children with diarrhea or malnutrition, as the rate of malnutrition among children has increased in Yemen due to the war that has been going on for 8 years and has not ended until now19.

Thus the study's main goal was to determine the prevalence of intestinal parasite infections among primary school students.

 

SUBJECTS AND METHODS 

 

Study design: Cross sectional study was carried out among primary schoolchildren.

Place and duration of study: The research was carried out at Sana'a University in Sana'a, Yemen, at the Faculty of Medicine and Health Sciences, Medical Microbiology and Parasitology departments. 400 fecal samples from 400 randomly chosen schoolchildren in Thala'a city, Amran governorate, aged 7 to 12, were tested between January and February 2022.

Analysis of samples: Following receipt of the samples in the lab, wet-mount preparations with saline and iodine were made and screened within two hours of sample collection to look for motile Trophozoites, larvae, eggs, and cysts. Fecal samples were also treated with a formalin-ether concentration technique and re-examined with wet saline-iodine preparations as well as stained with a modified acid-fast dye15 to look for Cryptosporidium, Cyclospora and Isospora oocysts. Each wet form and stained fecal swabs were examined by a clinical microbiologist and researcher (Prof. AMA) independently and the results verified.

Collection and analysis of Data:  Demographic data were collected in a standard questionnaire, and the results of intestinal parasites, helminthes, and coccidian parasites were analyzed and their association with demographic data were studied.

Ethical approval: The Medical Ethics Committee of the Faculty of Medicine and Health Sciences of Sana'a University gave its official permission on January 1, 2022, with  reference number 2022-11.

Ethical consideration: Consents were taken from all the participants and their families and the participants were informed that participation is voluntary and that they can refuse without giving any reason.

 

RESULTS

 

The study findings are represented in three tables. The children's ages ranged from 7 to 12 years, with a mean SD of 9.52 (2.9 years) (Table 1). The results showed that 136/400 (34%) of the tested children were positive for intestinal parasite infection, with a higher prevalence of specific intestinal worms (50.4%, n=133) than protozoa (33.3%, n=88) and coccidian infection (16.3%, n=43). The rate of infection alone was also higher than that of multiple parasitic infections (19.3% vs. 14.8%). 

The highest number of intestinal parasites were 12.5% (n=50) for A. lumbricoides and 12.25% (n=49) for E. histolytica, followed by 9.8% (n=39) for G. lamblia, 11.5% (n=46) for E. vermicularis, 6.5% (n=26) for Cryptosporidium species, 6.5% (n=26) for Hymenolepis nana, 2% (n=8) for S. mansoni, and 0.8% (n=3) for T. trichiura (Table 2). Considering the associated factors, boys had a higher infection rate than girls (50% vs. 24.2%), with an OR of 2.6 and a CI of 1.7–3.9 (p=0.05). A higher rate was also recorded in older children (41%, n=57), with an odds ratio of 1.6 (p=0.05) (Table 3).

 

DISCUSSION AND RECOMMENDATIONS

 

The current study showed that 34% of the children were infected with intestinal parasites. This score is lower than that previously reported in different regions of Yemen, including Hadramout (58.7%)20, Ibb (62.7%)21, Hajjah (58.8%)8, and Sana’a (54.8%)22, and is well below 90% among schoolchildren in Al-Mahweet Governorate23. The results of the current study revealed that intestinal worms were found in 50.4% of the patients, whereas intestinal protozoa were present in 33.3% of the cases. This data conflicts with that of Qasem et al.,21 who discovered that schoolchildren had protozoa and helminthes infections at rates of 85.64% and 14.36%, respectively. A. lumbricoides (12.5%) and E. histolytica (12.25%) were found to be the most prevalent intestinal protozoa, followed by Giardia lamblia (9.8%) and E. vermicularis (11.5%), according to the findings of the current study (Table 2). These results are in line with earlier studies conducted in Yemen, including one by Qasem et al.21, which discovered that E. histolytica, G. lamblia, and A. lumbricoides were the most prevalent intestinal parasites. Additionally, Alshahethi et al.,24,25 found that G. lamblia and E. histolytica were the most common intestinal parasites among schoolchildren in the Amran governorate. Boys had a greater infection rate than girls in the current study (50% vs. 24.2%), with an odds ratio of 2.6 and a confidence interval of 1.7–3.9 (p=0.001) when parasitism-related factors were taken into account. This result conflicts with research by Qasem et al., where it was shown that girls have a substantially greater infection rate than boys. Current findings, however, are consistent with those made public by Moghalli et al.,8 in Hajjah, where boys were more likely to contract the infection than girls. This could be explained by the excessive movement of boys and more exposure to eating habits outside the home and/or poor personal hygiene behavior compared to girls. The infection rate alone was also higher than the rate of multiple parasitic infections (19.3% vs. 14.8%), and multiple parasitic infections may lead to gastrointestinal bleeding, malabsorption of nutrients, nutritional deficiencies, and cell and tissue damage. Ultimately, these outcomes generally result in growth retardation, slow weight growth, decreased mental development, truancy, reduced academic performance and a predisposition to malnutrition and infection by other microorganisms23,26,27. Cryptosporidium, Isospora and Cyclospora are becoming increasingly prevalent in immunocompromised patients as well as in humans with normal immunity.

Humans can become infected with coccidiosis through the fecal-oral route, through direct person-to-person or animal-to-person contact as well as consumption of contaminated water or food27 while an animal reservoir for human Isospora has not yet been identified28. In the current study, the prevalence of Cryptosporidium spp was 6.5%, while Cyclospora spp was the second most common spherical pathogen (3.5%). The results of this study are lower than those reported among schoolchildren in Al-Turbah city, Taiz governorate, by Shamsan et al.,16 as the prevalence of Cryptosporidium spp, Cyclospora spp, and Isospora belli parasites reached 75.9%, 45.6%, and 1.75%, respectively18. However, the results of this study are similar to those reported in the general population of developing and developed countries where Cryptosporidium oocysts rate of less than 6%, was recorded29. Also, the current study rate of Cryptosporidium spp (6.5%) was lower than the prevalence rates of Cryptosporidiosis among HIV/AIDS diarrheal patients which ranged from about 10% to 33%29,30 but approximately similar to that among diarrheic children with normal immunity31.

In order of the present findings, however, many research-based interventions have mostly taken place in disadvantaged nations and regions, where sanitation is a key concern for disease prevalence8,16. Methods of preventing intestinal parasites are not isolated to certain geographic areas. Using correct hand washing techniques, using restrooms that are built properly and have enough ventilation, having a piped water source, and wearing shoes are some of the current best practices for preventing intestinal parasites32,33. Currently, up to 80% of the population does not have access to washing facilities in some areas of Yemen where the disease is most widespread. Even though this number is large, 93% of people have access to latrines, but only 29.2% of them are built properly to prevent parasite infection8,16,34.

Behavioral interventions focused on encouraging washing, sometimes with soap, in the context of education in schools and childcare facilities35. In recent studies, the best interventions take a multidisciplinary approach by: increasing environmental sanitation to promote hand-washing and shoe-wearing habits, and teaching children from an early age at school and at home. However, all that was mentioned has no effect in Yemen, and schools have become recruitment centers for children. Yemen also need particular evidence-based interventions, such as those in schools that concentrate on creating better restrooms with better ventilation, offering clean drinking water, and teaching kids about good hygiene36. A SAFE (Surgery, Antibiotics, face Hygiene, Environmental Sanitation) approach is used to treat trachoma, with a focus on environmental sanitation and face hygiene37. Cutting nails and washing hands with soap at key periods can both help to lower re-infection rates, but additional research is required before developing and implemen-ting these interventions on a wide scale. Programs that incorporate anthelmintic medication administration with measures to improve environmental cleanliness (such minimizing fecal pollution) also can be applicable in Yemen38.

Limitations of the study

This study has flaws since the samples were only analyzed using basic techniques, and modern genetic methods were not used to examine the samples. This is one of the things that may lower the accuracy and validity of the results.

 

CONCLUSION

 

The healthcare sector continues to have serious concerns about the high prevalence of intestinal parasite infections in youngsters. Intestinal parasite illnesses are common in low-income settings where environmental hygiene is poor and personal hygiene practices are lacking. Therefore, a variety of control strategies are needed to reduce and eventually eliminate the incidence of intestinal parasitosis among students. The report also emphasizes how common coccidian parasites are among Yemen's immuno-competent schoolchildren. Coccidian parasites, even in immunocompetent children, can cause childhood diarrhea, therefore Yemeni doctors need to be aware of this.

 

ACKNOWLEDGEMENTS 

 

The authors would like to thank the National Center for Public Health Laboratories (NCPHL) Sana'a, Yemen for the support.

 

CONFLICT OF INTEREST 

 

No conflict of interest associated with this work.

 

AUTHOR CONTRIBUTIONS

 

All authors contributed to fieldwork, lab work, data analysis, paper drafting and review, and gave final approval for the research.

 

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