|Year : 2018 | Volume
| Issue : 2 | Page : 78-85
Prevalence of enteric parasitic diseases among patients referred at a teaching hospital in Kenya
Rose Jepkosgei Kimosop1, Chrispinus Siteti Mulambalah1, Moses Mwajar Ngeiywa2
1 Department of Medical Microbiology and Parasitology, School of Medicine, College of Health Sciences, Moi University, Eldoret, Kenya
2 Department of Biological Sciences, School of Science, University of Eldoret, Eldoret, Kenya
|Date of Submission||04-Feb-2018|
|Date of Acceptance||22-May-2018|
|Date of Web Publication||13-Aug-2018|
Prof. Chrispinus Siteti Mulambalah
Department of Medical Microbiology and Parasitology, School of Medicine, College of Health Sciences, Moi University, P. O. Box: 4606-30100, Eldoret
Source of Support: None, Conflict of Interest: None
Aim: Enteric parasitic diseases pose a serious public health problem worldwide and yet are neglected. To refocus attention on these diseases, a cross-sectional study was conducted to assess the prevalence of enteric infections in patients referred to referral hospital in Kenya. Materials and Methods: This study was conducted from April to December 2015 and involved a randomly selected sample of 185 patients. Fecal specimens were collected and delivered to laboratory for analysis. Preliminary macroscopic assessment of specimens for segments, larvae, and adult stages was done. To confirm the presence of ova, trophozoites, cysts, and oocysts, direct wet smear, formol–ether concentration, and modified Ziehl–Neelsen techniques were used. Results: Overall prevalence of 46.5% of enteric parasitic diseases was confirmed. Highest and lowest prevalence was due to protozoans and helminthes, respectively. Protozoan parasite prevalence was Entamoeba histolytica (23.9%), Cryptosporidium parvum (13%), Entamoeba coli (6.5%), Giardia lamblia (6.5%), and Iodamoeba butschlii (6.5%). Helminth prevalence was Ascaris lumbricoides (1.6%), Hymenolepis nana, Trichuris trichiura, and Ancylostoma duodenale each (0.5%). There was no significant difference in prevalence in age groups and gender (P = 0.05). Females were at the highest risk of C. parvum infection. Polyparasitism was prevalent among protozoans than helminthes. Conclusion: High prevalence of protozoan infections was observed among referred patients in comparison to helminthiasis. Based on reported multiple infections, deworming programs targeting helminthiasis should be restructured to incorporate diagnosis and treatment of enteric protozoan infections to reduce prevalence of enteric parasitic infections.
Keywords: Amoebiasis, Ascariasis, Geohelminths, Giardiasis, Helminths, Protozoans
|How to cite this article:|
Kimosop RJ, Mulambalah CS, Ngeiywa MM. Prevalence of enteric parasitic diseases among patients referred at a teaching hospital in Kenya. J Health Res Rev 2018;5:78-85
|How to cite this URL:|
Kimosop RJ, Mulambalah CS, Ngeiywa MM. Prevalence of enteric parasitic diseases among patients referred at a teaching hospital in Kenya. J Health Res Rev [serial online] 2018 [cited 2018 Sep 24];5:78-85. Available from: http://www.jhrr.org/text.asp?2018/5/2/78/238865
| Introduction|| |
Intestinal parasitic infections caused by protozoa and helminthes are among the most widespread of human infections worldwide. These constitute the greatest single cause of illness and disease and are important threats to healthy living in both developed and developing countries., The world health organization estimates that approximately 60% of the world's population is infected with intestinal parasites known to play a significant role in morbidity and mortality. The infections, therefore, constitute one of the greatest single worldwide causes of illness and disease.
The prevalence is high in Sub-Saharan Africa due to poor sanitary habits, lack of access to safe water, and improper hygiene, and hence, these infections are often referred to as diseases of poverty. In many Africa countries, the prevalence of infections varies from one region and community to another due to various factors. This is in most cases is associated with contaminated environment and the sociocultural habits of communities.,,
The parasites involved are single-celled protozoans and multicellular helminthes of various species known to infect humans since prehistoric times and have evolved with man throughout history. The clinical presentation of diseases associated with the parasites varies depending on species but generally includes diarrheal illness caused by protozoans such as Entamoeba histolytica, Cryptosporidium parvum, Giardia lamblia, and intestinal helminthiases caused by geohelminths including nematodes and some trematodes.
Enteric protozoan infections are prevalent and constitute a major global infectious disease burden. The most common being amoebiasis caused by intestinal amoeba, E. histolytica, is an important parasitic disease worldwide, with the highest impact reported in developing countries.C. parvum has been consistently associated with diarrhea in HIV/AIDS worldwide.,G. lamblia, causative agent of giardiasis, is prevalent worldwide infecting an estimated 200 million people.,,Blastocystis hominis whose parasitic status is not clearly known has been reported in humans and its prevalence is not adequately documented.
The global prevalence of intestinal geohelminth infections is estimated to be over 1 billion cases of Ascaris lumbricoides, 740 million cases of Necator americanus and Ancylostoma duodenale, and 795 million cases of Trichuris trichiura. The four intestinal geohelminths occasionally occur concurrently in the community, resulting in multiple infections over a period of time, especially in children with serious adverse effects.
Intestinal parasitic infections have serious consequences on human health, such as swollen liver and spleen and intestinal bleeding. In spite of the current intervention strategies in Kenya and many other countries, the infections remain a major but neglected health problem, and yet, in most of the endemic areas, there is continued exposure. There is a need to encourage renewed interest and focus on these neglected tropical diseases.
Adverse effects including disabilities due to various intestinal parasitic infections are prevalent among patients who seek medical attention at county health facilities in Kenya that lack modern laboratory equipment and are inadequately staffed. The patients often present with nonspecific clinical manifestations and diagnosis based on clinical observations alone are often misleading and may lead to wrong treatment. Such inadequately managed infections, therefore, persist and most of the cases end up as referral cases at teaching hospitals for appropriate laboratory-based diagnosis and disease management. The aim of the study was to identify the specific enteric parasite species and assess the gender- and age group-related disease prevalence among patients referred to a teaching and referral hospital. The purpose of the study was to encourage renewed interest and focus on these neglected tropical diseases some of which have emerged as important opportunistic infections in the current AIDS pandemic and requires specific diagnostic testing and treatment approaches. Prevalence findings provide a basis for targeted approach for treatment based on evidence-based diagnostic test results. This is important in improving patient treatment outcome, rational use of drugs, and setting up of appropriate community-based specific intervention programs.,
| Materials and Methods|| |
Study site and setting
The study was conducted at referral hospital, located along Nandi road in Eldoret town, 310 km northwest of Nairobi city, Kenya. It is the second largest national hospital and the main referral facility in Uasin Gishu County and in the North Rift region of western Kenya. The hospital has 800-bed capacity and is a teaching and referral facility that receives patients from western Kenya, parts of eastern Uganda, and southern Sudan. The hospital offers a wide range of specialized services to both outpatients and inpatients. The hospital has modern state of the art clinical and diagnostic equipment manned by qualified and experienced medical, paramedical, and support staff from the hospital and the college of health sciences.
Study design, population, and sample size
This was an analytical cross-sectional study conducted from April 1 to December 31, 2015. The study population consisted of all consenting age groups and sexes who were referred to the laboratory for stool analysis. All willing participants were advised on how to collect fresh stool specimen without contamination and were provided with the polypots. They were instructed to collect fresh stool and deliver it immediately to the parasitology diagnostic laboratory.
Basing on previous related studies, the sample size was calculated at 95% confidence level and 5% marginal error. The study sample size (n) was estimated using modified Fisher's formula as used by Mugenda and Mugenda.
n = z2pq/d2
n = Desired sample size
z = Standard normal deviate (1.96)
p = Prevalence of intestinal parasites from previous study of 13.7%
q = 1.0 − p
d = Degree of accuracy
n = (1.96)2 (0.14) (1.0–0.14)/(0.05)2
n = 185 patients.
Therefore, the minimum sample size aimed at was 185 patients.
The study participants were categorized into the age groups: <9 years, 10–19 years, 20–29 years, 30–39 years, 40–49 years, and 50 and beyond years.
Inclusion and exclusion criteria
All patients who were sent to the laboratory for stool analysis and consented by signing the provided form were included in the study. Patients of unsound mind and those whose parents/guardians did not consent were excluded from the study.
The study protocol was approved by the Institutional Research and Ethics Committee approval reference number 0001601. The purpose and benefit of the study were explained to the patients through informed verbal consent before signing the consent form. For participants below the legal age of 18 years, consent was obtained from parents/guardians before considered for enrollment in the study.
For confidentiality, all participants were identified by specific codes and none of them was identified by name. There was no monetary benefit or any form of inducement for participation in the study. However, patients diagnosed positive with intestinal parasites were referred to a clinician for treatment and management. All individuals in the population were recruited regardless of age, ethnic origin, education, marital status, or social status so long as consent was obtained.
Collection and preservation of stool specimens
All consenting patients were given a dry, clean, leak-proof plastic container labeled with the serial code age, date and gender for identification, and a wooden scoop for the collection of stool specimen. They were guided on how to collect the specimen appropriately. In the case of children, stool was collected immediately after defecation and specimen put into the sample bottle. They were advised to fill half the container and safely discard the scoop after use. The stool specimens were delivered to the laboratory for processing.
Once specimens were received in the medical parasitology laboratory, they were either processed or preserved in 10% formalin until Formol-ether concentration technique was performed. Preservation of the specimens was essential for maintenance of protozoal morphology and also to prevent further development of helminthic eggs and larvae and thus render the specimens safe.
Specimen processing and identification of parasites
Immediately after delivery in laboratory, all stool specimens were examined macroscopically for adult and the larval stages of helminth parasites. Further, the specimens were analyzed microscopically for the presence of trophozoites, ova, oocysts, and cysts using both direct saline and iodine mounts on clean grease-free slides. Slides were then prepared directly for wet mount in saline as well as in iodine and were microscopically examined for helminth cysts or eggs and protozoan parasites.
Detection and identification of protozoal cysts and helminth eggs were achieved by formol–ether concentration technique. One gram of stool specimen was fixed by emulsifying in 7 ml of 10% formal saline and kept for 10 min. It was then strained through a wire gauge and the filtrate was collected in a centrifuge tube. Three milliliters of ether was added to it and the mixture was shaken vigorously for 1 min. It was then centrifuged at 2000 rpm for 2 min and then allowed to settle. The debris was loosened with a stick; the upper part of the test tube was cleared of fatty debris; and the supernatant fluid was decanted, leaving 1 or 2 drops. The deposit, after shaking, was poured on to a glass slide, and a cover slip placed over it and the specimen was examined microscopically.
Modified Ziehl–Neelsen (Z-N) technique was used to identify coccidian oocysts in stool specimens. Stool smears were prepared from the concentrated stool specimen; air dried and stained by the modified Z-N staining technique for identification of oocysts of Cryptosporidium species, Isospora belli, and Cyclospora cayetanensis following the method described by Cheesbrough (1985). The smears were fixed with methanol for 10 min and 7 drops of carbol fuchsin were flooded for 3 min. Decolorization was done with 5% sulfuric acid for 30 s. Then, it was counterstained with methylene blue for a minute. The smear was rinsed, drained, air-dried, and examined under oil immersion power. This diagnostic technique is the most suitable for demonstration of oocysts of the protozoans. Microscopy was done first with power (×40 = 400 times magnification) to determine the distribution then power (×100 = 1000 times magnification) bright field for identification. For each batch of smears which was processed through the modified Z-N stain, positive control was included for quality assurance. Each sample was observed microscopically by two other technologists for confirmation and verification before declaring the final result.
Quality assurance and data analysis
To ensure quality results, only trained, qualified, and experienced research assistants were engaged in the study. It was mandatory for slide preparations to be checked by three different observers before declared negative. A third of the slides was randomly selected and sent to the Department of Medical Microbiology and Parasitology, School of Medicine, for results' verification quality assurance.
All data were checked for accuracy before it was entered into and analyzed using SPSS incorporation for windows, version 16.0. (Chicago, USA). Descriptive and inferential statistics such as mean median, standard deviations, and ranges were carried out for continuous data while frequency listing and percentages were used to explore categorical data. Prevalence was calculated for each identified parasite species and association between categorical variables such as the gender status assessed using Chi-square test. In all analyses, P < 0.05 was considered statistically significant.
| Results|| |
Participant's characteristics and identified parasites
A total of 185 participants were enrolled in the study translating into 104 (56.2%) females and 81 (43.8%) males. The participants had an age range of between 2 and 70 years with a mean age of 24. The total number of patients who were diagnosed positive for parasitic infections was 86 (46.5%). The number of positive cases due to protozoans was 103 (56%) while those diagnosed with intestinal helminthiases was 7 (6.4%). The identified protozoan and helminth parasite species are presented in [Table 1].
Enteric parasitic infection distribution in age groups
Amoebiasis was the most prevalent infection across all age groups in all referred cases. The prevalence was low (3.7%–12.9%) in the lower age groups than in the elderly (25%). However, there was no significant difference in prevalence between the age groups (P = 3.525). Cryptosporidiosis had moderate prevalence but sufficient to cause concern because of its current status as important opportunistic infection in HIV/AIDS patients. Both cryptosporidiosis and giardiasis occurred as low prevalence infections in all age groups except the elderly and there was no significant difference between age groups (P = 1.160). The age group-related protozoal and helminth infection prevalence distribution is presented in [Table 2].
Comparison of age group- and gender-related parasitic infections
Overall, of the two categories of enteric infections (protozoal and helminth infections), protozoal infections were the most prevalent in all age groups and both genders. Under this category, amoebiasis was the most common infection in all ages and gender, while cryptosporidiosis and giardiasis were the least prevalent. However, cryptosporidiosis had a higher infection rate in females than males whereas amoebiasis was more prevalent in males than females.
Compared to protozoal infections, intestinal helminth infections were least prevalent in age groups and both genders. Whereas protozoal infections were spread across all age groups, no positive cases of helminthiasis were recorded in lower and upper age groups. This implies that helminthiasis was only prevalent in middle age groups (10–39 years) of the referred cases. Low-level prevalence of helminthiasis was recorded in both genders. No cases of giardiasis, cryptosporidiosis, and helminthiasis were detected in referred patients' age >50 years. In general, the prevalence of the parasitic infections was higher in males than females, but this difference was not statistically significant (P > 0.05). Comparative age group- and gender-related prevalence is presented in [Table 3].
Multiple intestinal infections were 6.4% prevalent in the referred cases with the most common combinations being protozoan species E. histolytica and Entamoeba coli, E. histolytica and Iodamoeba butschlii. Arare combination of A. duodenale and I. butschlii was also recorded. There was no statistically significant difference in the number with single and multiple infections (P = 0.562). Polyparasitism was not specific to a particular age group or gender.
| Discussion|| |
A variety of protozoan and helminth parasite species were identified from referred patients and confirmed as causative agents of gastrointestinal problems and general ill health. The study findings confirm that overall, protozoan parasites were the main cause of enteric infections among referred cases. The parasite species E. histolytica, E. coli, I. butschlii, and G. lamblia accounted for over 55% of all infections associated with protozoans compared to intestinal helminths at 7%. This is comparable to related studies., In these studies, the prevalence of intestinal parasitic infection by protozoa ranged 33%–53%. On the other hand, our findings are in disagreement with studies done elsewhere. The findings in these studies indicate protozoan prevalence as low as 13.2% to 34% and that of helminth infections as 26.9%.,, The variance could be explained by application of different diagnostic tests and variations in sample size and selection procedures and participant inclusion and exclusion criteria.
Amoebiasis caused by E. histolytica was the most prevalent protozoal infection in all age groups (3.7%–25%) and both genders (27.6%–36.2%). This suggests that all ages and genders are susceptible to infection. The findings are in agreement with related studies in developing and developed countries.,, Further, related studies reveal similar trend in amoebiasis gender-related prevalence, for instance, Nepal (17%–22%), Brazil (26%–30%), and Ethiopia (32%–36%).,, Exceptionally higher rates of amoebiasis infection in males and females have been reported elsewhere in Africa (60%–64%) and other regions of Kenya (48%–52%)., In these studies, fairly large samples collected for longer period were used. This is also suggestive of sustained environmental contamination and poor hygiene which enhances continuous infection and re-infection.
The high prevalence of amoebiasis suggests that the infection transfer between and among persons through food or water is high. This is an indication of high-level fecal contamination by animal reservoir hosts and humans. The human role in this aspect is further supported by reported high number of asymptomatic cases in general population that constitute source of infection to others without suffering ill health. In addition, the high prevalence of E. histolytica could be due to the double-walled resistant cysts of the parasite which can withstand and survive adverse environmental including chemical water treatment.
The 13% prevalence of cryptosporidiosis was comparable with other related studies in Africa., However, this prevalence was lower compared to 32%–67% reported in immunosuppressed and symptomatic subjects., This re-emphasizes the importance of C. parvum as an intestinal opportunistic infection. The high prevalence rate of 33% recorded in the females in the 40–49 years' age group may to some extent be attributed to age-related weakened immunity and autoinfection due to repeated exposure to infective oocysts. Further, in African setting, it is the women who take care of the sick including HIV/AIDS victims at home. In this regard, close contact while taking care of patients enhances probability of transmission through accidental ingestion of oocysts in contaminated water or food. It is possible that cases of cryptosporidiosis are underestimated and therefore not adequately documented because modified Z-N test is not routinely used in most of the hospital laboratories at county level. Such cases including healthy carriers remain continuous source of infection in a community unless referred to facilities with modern diagnostic facilities.
Compared to other enteric protozoal infections, giardiasis has the lowest prevalence (1.6%–3.7%) across all age groups and gender except patients >50 years. This is low prevalence compared to similar study in which prevalence of 20%–30% was reported. However, in both studies, there was evidence of giardiasis persistence in the community. This phenomenon could be attributed to animal reservoirs, cross-infectivity between animals and humans, and asymptomatic individuals and possibly involvement of several parasite species and strains. The net effect is increased risk of transmission in all age groups and gender and therefore a possible explanation for the cosmopolitan nature of giardiasis which may in the near future emerge as an opportunistic infection., The nonpathogenic protozoa found in all age groups were E. coli and I. butschlii.
The prevalence of ascariasis and trichuriasis was low (0.5%–1.6%) comparable with several similar studies.,,, It is possible that the ova of these nematodes require further development outside the host before becoming sufficiently infective. In harsh environment (dry soil contaminated with pesticides and chemical fertilizers), many of the ova die and become noninfective even if ingested. The few ova that survive are probably the ones responsible for the low infection prevalence. In related studies, either none or very few cases of the two parasites have been reported., However, isolated reports of prevalence exceeding 12% have been documented., The overall low prevalence of intestinal helminthiasis in the study is possibly indicative of a positive outcome of ongoing school-based deworming program at county level. Diagnosis and treatment of school children accompanied with community health education could explain the low rate of intestinal helminthiasis reported elsewhere.
The present study findings indicate an equal exposure of both genders to enteric parasitic infections. This suggests that these infections may be associated with everyday activities of individuals rather than gender. Therefore, under shared similar environmental conditions, gender has no influence on the prevalence of enteric parasitic infections. Nevertheless, age has a profound effect on infections. Children who most often have a tendency to eat food without hand washing unless reminded or may lick contaminated fingers end with higher rates of infection compared to adults. Furthermore, the age group comprises individuals who are increasingly involved in outdoor activities including handling items likely to be fecal contaminated which predispose them to parasitic infections.
Cases of polyparasitism were more prevalent among intestinal protozoa and rare between intestinal helminthes and protozoans. Even though the parasites in the study share similar external and internal environmental conditions and all are feco-orally transmitted, the rare occurrence of polyparasitism involving helminthes and protozoa needs further investigation.
| Conclusion|| |
Based on the study findings, E. histolytica and G. lamblia were the most prevalent pathogenic intestinal protozoa and major contributors to ill health and diarrheal disease while A. lumbricoides, A. duodenale, and T. trichiura were less common in patients referred to teaching and referral hospital.
All age groups were susceptible to enteric parasitic infections but at different rates. The most prevalent parasitic infections were amoebiasis, cryptosporidiosis, and giardiasis.
Both genders were susceptible to infection with protozoal and helminth parasites, though among the protozoal infections, cryptosporidiosis was more prevalent in females than males.
Cases of polyparasitism involving protozoans were common while a combination of protozoa and helminthes was rare.
Considering that all the parasites in the study are feco-orally transmitted and confirmation of polyparasitism, we conclude that faecally polluted environment and poor sanitary conditions lead to continuous infection and re-infection in the community. These together with the reported prevalence rates of enteric parasitic infections among the referred cases suggest that the infections constitute a major a public health problem.
We recommend that since provision of health services is a devolved function in Kenya since 2010, the regional governments should focus more attention on: community-based health promotions with a component on regular checkups and treatment of enteric parasitic infections; provide modern and appropriate diagnostic equipment and laboratories and scale up deworming programs; provide clean water for domestic use; and improve on environmental hygiene and human waste disposal.
The authors appreciate and thank Mr. Siteti Darwin Injete of Jomo Kenyatta University of Agriculture and Technology who reviewed the paper and offered constructive suggestions.
Financial support and sponsorship
The authors acknowledge the Flemish Interuniversity Council University Development Co-operation, Belgium for financial support.
Conflicts of interest
There are no conflicts of interest.
| References|| |
Strunz EC, Addiss DG, Stocks ME, Ogden S, Utzinger J, Freeman MC, et al.
Water, sanitation, hygiene, and soil-transmitted helminth infection: A systematic review and meta-analysis. PLoS Med 2014;11:e1001620.
World Health Organization. Investing to overcome the global impact of neglected tropical Diseases: Third WHO report on neglected diseases. Geneva, Switzerland: WHO Press; 2015. p. 1-191.
Amoah ID, Singh G, Stenström TA, Reddy P. Detection and quantification of soil-transmitted helminths in environmental samples: A review of current state-of-the-art and future perspectives. Acta Trop 2017;169:187-201.
Bekele F, Tefera T, Biresaw G, Yohannes T. Parasitic contamination of raw vegetables and fruits collected from selected local markets in Arba Minch town, Southern Ethiopia. Infect Dis Poverty 2017;6:19.
Speich B, Croll D, Fürst T, Utzinger J, Keiser J. Effect of sanitation and water treatment on intestinal protozoa infection: A systematic review and meta-analysis. Lancet Infect Dis 2016;16:87-99.
O'Connell EM, Nutman TB. Molecular diagnostics for soil-transmitted helminths. Am J Trop Med Hyg 2016;95:508-13.
Cleaveland S, Laurenson MK, Taylor LH. Diseases of humans and their domestic mammals: Pathogen characteristics, host range and the risk of emergence. Philos Trans R Soc Lond B Biol Sci 2001;356:991-9.
Alemu A, Tegegne Y, Damte D, Melku M. Schistosoma mansoni
and soil-transmitted helminths among preschool-aged children in Chuahit, Dembia district, Northwest Ethiopia: Prevalence, intensity of infection and associated risk factors. BMC Public Health 2016;16:422.
O'connor RM, Shaffie R, Kang G, Ward HD. Cryptosporidiosis in patients with HIV/AIDS. AIDS 2011;25:549-60.
Sparks H, Nair G, Castellanos-Gonzalez A, White AC Jr. Treatment of Cryptosporidium
: What we know, gaps, and the way forward. Curr Trop Med Rep 2015;2:181-7.
Heyworth MF. Giardia duodenalis
genetic assemblages and hosts. Parasite 2016;23:13.
Yoder JS, Gargano JW, Wallace RM, Beach MJ; Centers for Disease Control and Prevention (CDC). Giardiasis surveillance – United states, 2009-2010. MMWR Surveill Summ 2012;61:13-23.
Kurt Ö, Doğruman Al F, Tanyüksel M. Eradication of Blastocystis
in humans: Really necessary for all? Parasitol Int 2016;65:797-801.
Darlan DM, Tala ZZ, Amanta C, Warli SM, Arrasyid NK. Correlation between soil transmitted helminth infection and eosinophil levels among primary school children in Medan. Open Access Maced J Med Sci 2017;5:142-6.
Alelign T, Degarege A, Erko B. Soil-transmitted helminth infections and associated risk factors among schoolchildren in Durbete town, Northwestern Ethiopia. J Parasitol Res 2015;2015:641602.
Abu-Madi MA, Behnke JM, Boughattas S, Al-Thani A, Doiphode SH. A decade of intestinal protozoan epidemiology among settled immigrants in Qatar. BMC Infect Dis 2016;16:370.
World Health Organization. Model Prescribing Information: Drugs Used in Parasitic Diseases-Second Edition: Helminths: Cestode (Tapeworm
) Infection. Available from: http://www. Apps. Who. Int
. [Last accessed on 2017 Dec 09].
Mugenda OM, Mugenda AG. Research Methods: Quantitative and Qualitative approaches. Kenya, Nairobi: African Center of Technology Studies; 1999.
Cheesbrough M. District Laboratory Practice in Tropical Countries-Part-1. New York: Cambridge University Press; 2009. p. 29-35.
Cheesbrough M. Medical Laboratory Manual for Tropical Countries. 2nd
ed., Vol. 1. Cambridge, UK. Butterworth and Company (pub) Ltd., Cambridge University Press; 1987. p. 181-6, 204-5, 217.
Ashtiani MT, Monajemzadeh M, Saghi B, Shams S, Mortazavi SH, Khaki S, et al
. Prevalence of intestinal parasites among children referred to Children's Medical Center during 18 years (1991-2008), Tehran, Iran. Ann Trop Med Parasitol 2011;105:507-12.
Mehraj V, Hatcher J, Akhtar S, Rafique G, Beg MA. Prevalence and factors associated with intestinal parasitic infection among children in an urban slum of Karachi. PLoS One 2008;3:e3680.
Gelaw A, Anagaw B, Nigussie B, Silesh B, Yirga A, Alem M, et al
. Prevalence of intestinal parasitic infections and risk factors among schoolchildren at the University of Gondar Community school, Northwest Ethiopia: A cross-sectional study. BMC Public Health 2013;13:304.
Nduka FO, Nwaugo VO, Nwachukwu NC. Human intestinal parasite infections in Ishiagu, a leading mining Area of Abia State. Anim Res Int 2006;3:505-7.
Wongstitwilairoong B, Srijan A, Serichantalergs O, Fukuda CD, McDaniel P, Bodhidatta L, et al
. Intestinal parasitic infections among pre-school children in Sangkhlaburi, Thailand. Am J Trop Med Hyg 2007;76:345-50.
Manganelli L, Berrilli F, Di Cave D, Ercoli L, Capelli G, Otranto D, et al
. Intestinal parasite infections in immigrant children in the city of Rome, related risk factors and possible impact on nutritional status. Parasit Vectors 2012;5:265.
Abbas OF. Prevalence of intestinal parasitic infestations in Al-Anbar Province, West of Iraq. J Univ Anbar Pure Sci 2012;6:12-5.
Mukhiya RK, Rai SK, Karki AB, Prajapati A. Intestinal Protozoan
parasitic infection among school children. J Nepal Health Res Counc 2012;10:204-7.
Nobre LN, Silva RV, Macedo MS, Teixeira RA, Lamounier JA, Franceschini SC, et al
. Risk factors for intestinal parasitic infections in preschoolers in a low socio-economic area, Diamantina, Brazil. Pathog Glob Health 2013;107:103-6.
El Fatni C, Olmo F, El Fatni H, Romero D, Rosales MJ. First genotyping of Giardia duodenalis
and prevalence of enteroparasites in children from Tetouan (Morocco). Parasite 2014;21:48.
Mbae CK, Nokes DJ, Mulinge E, Nyambura J, Waruru A, Kariuki S, et al
. Intestinal parasitic infections in children presenting with diarrhoea in outpatient and inpatient settings in an informal settlement of Nairobi, Kenya. BMC Infect Dis 2013;13:243.
Fernandez MC, Verghese S, Bhuvaneswari R, Elizabeth SJ, Mathew T, Anitha A, et al
. A comparative study of the intestinal parasites prevalent among children living in rural and urban settings in and around Chennai. J Commun Dis 2002;34:35-9.
Yilmaz H, Tas-Cengiz Z, Cicek M. Investigation of cryptosporidiosis by enzyme-linked immunosorbent assay and microscopy in children with diarrhea. Saudi Med J 2008;29:526-9.
Vahedi M, Gohardehi S, Sharif M, Daryani A. Prevalence of parasites in patients with gastroenteritis at east of Mazandaran province, Northern Iran. Trop Biomed 2012;29:568-74.
Sanad MM, Al-Malki JS. Cryptosporidiosis among immunocompromised patients in Saudi Arabia. J Egypt Soc Parasitol 2007;37:765-74.
Al-Braiken FA, Amin A, Beeching NJ, Hommel M, Hart CA. Detection of Cryptosporidium
amongst diarrhoeic and asymptomatic children in Jeddah, Saudi Arabia. Ann Trop Med Parasitol 2003;97:505-10.
White AC Jr. Cryptosporidiosis (Cryptosporidium). In: Bennett JE, Dolin R, Blaser MK, editors. Principles and Practice of Infectious Diseases
. Ch. 284. Philadelphia, Pa: Elsevier Churchill Livingstone; 2015. p. 3173-83.
|40.|Scallan E, Hoekstra RM, Augulo FJ, Tauxe RV, Widdowson MA, Roy SL, et al. Foodborne illness acquired in the United States major pathogens. Emerg Infect Dis 2011;17:7-15.
Patel PK, Khandekar R. Intestinal parasitic infections among school children of the Dhahira Region of Oma. Saudi Med J 2006;27:627-632.
Al-Braiken FA. Is intestinal parasitic infection still a public health concern among Saudi children? Saudi Med J 2008;29:1630-5.
Al-Megrin WA. Intestinal parasites infection among immunocompromised patients in Riyadh, Saudi Arabia. Pak J Biol Sci 2010;13:390-4.
Sharif M, Daryani A, Asgarian F, Nasrolahei M. Intestinal parasitic infections among intellectual disability children in rehabilitation centers of Northern Iran. Res Dev Disabil 2010;31:924-8.
Bhutta ZA, Sommerfeld J, Lassi ZS, Salam RA, Das JK. Global burden, distribution, and interventions for infectious diseases of poverty. Infect Dis Poverty 2014;3:21.
Fenwick A, Jourdan P. Schistosomiasis elimination by 2020 or 2030? Int J Parasitol 2016;46:385-8.
Muñoz-Antoli C, Pavón A, Marcilla A, Toledo R, Esteban JG. Prevalence and risk factors related to intestinal parasites among children in department of Rio San Juan, Nicaragua. Trans R Soc Trop Med Hyg 2014;108:774-82.
Sinniah B, Hassan AK, Sabaridah I, Soe MM, Ibrahim Z, Ali O, et al
. Prevalence of intestinal parasitic infections among communities living in different habitats and its comparison with one hundred and one studies conducted over the past 42 years (1970 to 2013) in Malaysia. Trop Biomed 2014;31:190-206.
Lo NC, Bogoch II, Utzinger J, Andrews JR. Cost-effectiveness of community-wide treatment for helminthiasis – Authors' reply. Lancet Glob Health 2016;4:e157-8.
[Table 1], [Table 2], [Table 3]