INTESTINAL PARASITES AND HELICOBACTER PYLORI ISOLATED FROM STOOL

SAMPLES OF DIARRHEIC AND NON-DIARRHEIC PATIENTS AT JARAMOGI ODINGA

TEACHING AND REFERRAL HOSPITAL IN KISUMU COUNTY

BY

HANNAH WANJIRU KAHORO

UBSM/17-A/020

A RESEARCH PROPOSAL SUBMITTED TO THE DEPARTMENT OF MICROBIOLOGY,

FACULTY OF HEALTH SCIENCES IN PARTIAL FULFILLMENT OF THE

REQUIREMENTS FOR THE AWARD OF BACHELOR'S DEGREE IN MICROBIOLOGY

AT UZIMA UNIVERSITY

MARCH 2021
 KISUMU -KENYA

DECLARATION

I declare that this research proposal is my own original work and has not been submitted to any

University for award of degree or any other award

Student Name: Kahoro Hannah Wanjiru

Reg No: UBSM/17-A/020

Signature…………………………………………….

Date of submission……………………….

Head of Microbiology Department: Dr Clement Shiluli,

Signature……………………………………

Date…………………………

Head of Research department: Mr Philip Nyaswa

Signature……………………………………………………

Date……………………………………………………….
ABBREVIATIONS

JOOTRH Jaramogi Odinga Teaching and Referral Hospital

WHO World Health Organisation

E. histolytica Entamoeba histolytica

G lamblia Giardia lamblia

A Lumbricoide Ascaris lumbricoides

T.trichura Trichuris trichiura

H.nana Hymenolepsis nana

S.mansomi schistosoma mansomi

H pylori Helicobacter pylori

List of Tables

Table 1.1- Budget

Table 1.2- Workplan

Table of Contents

DECLARATION 2
List of Tables 5
1.0 CHAPTER ONE 9
1.1 Introduction 9
1.2 Problem statement 11
1.3 Justification of the study 12
1.4 Main objective 13
1.4.1 Specific objective 13
1.4.2 Research questions 13
2.0 CHAPTER TWO-LITERATURE REVIEW 14
2.1 Introduction 14
2.2 Intestinal protozoan infections 14
2.2 Intestinal parasitic helminthes 16
2.3 Helicobacter pylori 17
3.0 CHAPTER THREE-METHODOLOGY 19
3.1 study population 19
3.2 study site 19
3.3 study design 20
3.4 sampling 21
3.5 sample size estimation 21
3.6 inclusion/exclusion criteria 21
3.7 lab methods 22
3.8 Data analysis 25
3.9 Ethical clearance 25
Abstract

Helicobacter pylori is among the most common infections in humans and has been recognized

to cause gastroduodenal diseases where opportunistic intestinal infections are known to cause

diarrhea especially in immunocompromised patients and this has become a significant act health

problem worldwide. H. pylori is a microaerophilic organism that causes chronic gastritis and

gastric ulcers. It is also linked to the development of duodenal ulcers and stomach cancer,

conditions that were not previously believed to have a microbial cause . This study aims to assess

and determine the prevalence of H pylori and intestinal parasites in patients representing with

gastroduodenal diseases with or without diarrhea at JOOTRH. Stool samples will be collected

from 298 patients who will present gastroduodenal diseases with or without diarrhea at JOOTRH

and be referred to microbiology laboratory. This stool samples will be examined for the presence

of protozoa, helminths and H pylori. The H. pylori stool antigen test will be performed on the

stool samples whereas formal ether sedimentation and direct method will be used to test

helminths and protozoa. Data will be analyzed used SPSS version 25.0 software and the result

will be presented in descriptive measures such as tables and figures. The findings of this study

will give the authorities in health sector a good chance to put in place adequate preventive

measures against H. pylori infection, helminths and protozoa. Importantly, all confirmed cases of

H. pylori, helminths and protozoa infection will be treated to avoid the chances of transmission.
1.0 CHAPTER ONE

1.1 Introduction

Human intestinal parasitic infections are among the most common infections in the world and are

responsible for considerable morbidity and mortality (la Hoz RM et al., 2019). Apart from

causing mortality and morbidity, infection with intestinal parasites has been associated with

malnutrition, stunting of linear growth and physical weakness in general. Intestinal parasitic

infections mainly manifest clinically in the form of diarrhea (Idris et al,2010) This is diagnosed

by an increased loss of stool with a frequency and fluidity higher than the usual for an individual

(Schiller et al,2014).

Helicobacter pylori infection is globally accepted as a major public health problem, with high

burden in African countries (Mohanna et al.,2014). In most cases, it is the cause of acute and

chronic gastritis and highly associated to gastric cancer and peptic ulcer. The inflammation in the

lining of the stomach or duodenum is the combined effect of stomach acid and H. pylori, which

leads to peptic ulceration. Although the route of transmission of H. pylori infection is not clearly

known, some evidences indicate that fecal contaminated water and food, fecal-oral contact and

kissing are source of infection. (Kimanga et al.,2010)

Children and young adults are the most affected, particularly in regions with limited sources and

where hygienic measures are not strictly followed (Gebretsadik et al., 2018). They are often the

most severe and deadly among children due to their small body size, and rapid ability to become

dehydrated (Peterson, 2008).

The age at which this bacterium is acquired seems to control the possible pathologic outcome of

the infection: individuals who are infected with H. pylori at an early age are likely to develop

more intense inflammation that may well be followed by atrophic gastritis with a higher

subsequent risk of gastric ulcer, gastric cancer or both (Mitchell et al., 2003).

Over 3.4 million people worldwide die every year due to parasitic diarrheal diseases associated

with inadequate sanitation and clean water (Conant, 2005) Many of the risk factors for

contracting diarrheal illnesses are associated with poor socioeconomic conditions, such as

lacking access to safe water and sanitation, poor hygiene practices and unsafe human waste

disposal (Bizuneh et al 2017).

In Addis Ababa, a study done on the prevalence of intestinal parasites in patient with and without

diarrhea in selected hospitals reaffirmed that opportunistic parasites can cause diarrhea most

common in pediatric patients. Among the opportunistic intestinal parasites that were associated

with diarrhea were Cryptosporidium parvum, Isospora belli, Ascaris lumbricoides, Trichurus

trichiura, Giardia lamblia and Entamoeba histolytica. (Adam et al 2006).

In Ethiopia, study done to determine the prevalence of intestinal parasites among HIV infected

individuals with or without diarrhea, showed high prevalence of protozoa and helminthes in the

study population. Cryptosporidium spp, E. histolytica, G lamblia, A Lumbricoides, T.trichura

and H.nana were among the opportunistic intestinal parasites that were associated with diarrhea

among HIV Patients (Mesfun et al 2019)

In Kenya, incidences of H. pylori infection is overwhelming high (Kimang‘a et al., 2010). The

increasing evidence of the incidences links the infection of gastric mucosa by H. pylori with

subsequent development of the gastric pathologies (Kimang‘a et al., 2010). However, more than
80 percent of persons who become infected with the bacterium are usually asymptomatic and it

have been suggested that it might take part in a vital role in the natural stomach ecology

(Kaakoush et al., 2015)

Epidemiology survey conducted at Mbagathi district hospital, Nairobi to determine the

prevalence of intestinal parasites in diarrheic children showed that, 25% of the samples were

positive for at least one parasite, with common parasites being Entamoeba histolytica (36%)

Cryptosporidium spp (30%) Giardia lamblia (16%). These parasites were associated with

diarrhea among the patients (Mbae et al 2013)

Diarrhea is still a global concern particularly in areas with limited access to safe and clean water,

poor sanitation and hygiene, with no exception of the study area. The relationship between

intestinal parasites and the high prevalence rate of diarrhea has not yet been clarified (Delahoy et

al 2012).

In Kisumu, minimal studies have been done to understand the prevalence of these intestinal

parasites and Helicobacter pylori in diarrheic and non-diarrheic patients. This study, thus, aims to

isolate and identify helminths, protozoa and H pylori in patients who present with

gastroduodenal diseases which might be the leading cause of diarrhea in patients visiting

diarrhea.

1.2 Problem statement

Intestinal parasites and H pylori are a burden to provision of healthcare in resource limited

settings. Despite efforts by WHO to eradicate intestinal parasitic infections and h pylori related

illnesses, infections continue to be persistent and affect a third of the population yearly in the
developing countries. Proper diagnosis and treatment of patients presenting with or without

diarrhea depends on the correct identification of parasites and bacteria, this will help in treatment

with the correct antacid and antiparasitic drugs. Therefore, data from this study could be used in

providing treatment guidelines for patients presenting with diarrhea at JOOTRH.

1.3 Justification of the study

The prevalence of intestinal parasites has been high in low- and middle-income countries with

demographic changes, increasing urbanization and poor hygiene practices. No firm and

consistent policy exists on the control of intestinal infections compared to other tropical and

infectious infections. Identification of intestinal parasites is necessary to reduce the rigorous and

strenuous process of diagnosis in resource strained hospitals.

Helicobacter pylori is among the most common infection in humans and has been recognized as

a major cause of gastroduodenal disease. There is increasing evidence that H pylori infects more

people in developing countries than in industrialized countries.

Knowledge of the prevalence of H pylori in patients presenting with gastroduodenal diseases will

help our understanding on how this infection is acquired locally. This knowledge can lead to

better planning of health science provisions making available the diagnostic tests used in

identifying H pylori and also providing H pylori eradication drugs for those who are

symptomatic. Public health measures can also be instituted to prevent the transmission of this

bacteria and hence reducing the disease burden.

There is paucity data on the prevalence of H pylori and intestinal parasites in the hospital. This

study therefore aims to obtain information on H pylori and intestinal parasites.

1.4 Main objective

To determine the prevalence of intestinal parasites and H pylori in stool samples obtained from

patients presenting with or without diarrhea at Jaramogi Odinga Teaching and Referral Hospital.

1.4.1 Specific objective

1. To determine the prevalence of parasitic protozoa in stool samples obtained from patients

presenting with diarrhea at JOOTRH

2. To determine the prevalence of helminthes in stool samples obtained from patients

presenting with diarrhea at JOOTRH.

3. To determine the prevalence of H pylori in stool samples obtained from patients

presenting with symptoms of gastroduodenal diseases

1.4.2 Research questions

a) What is the prevalence of parasitic protozoa in stool samples obtained from patients

presenting with diarrhea in JOOTRH?

b) What is the prevalence of helminthes in stool samples obtained from patients presenting

with diarrhea at JOOTRH?

c) What is the prevalence of H pylori in stool samples obtained from patients presenting

with symptoms of gastroduodenal diseases?

2.0 CHAPTER TWO-LITERATURE REVIEW

2.1 Introduction

Intestinal parasitic infections enjoy a wide global distribution. They are estimated to affect

3.5 billion people, most of whom are children residing in developing countries. The major

intestinal parasites of global health concern are the protozoa species Entamoeba histolytica

and Giardia intestinal is and soil transmitted helminths Ascaris lumbricoides, Trichuris

trichura and Hookworm which are opportunistic parasites causing diarrhea (Sitotaw at

al.,2017).

According to WHO more than 1.5 billion people are infected with particularly soil

transmitted helminths infections including 270 million preschool going children and over 600

million school age children (WHO 2016). Amoebiasis, giardiasis, ascariasis, hookworm and

trichiasis are the most common infections leading to diarrhea (Rashid et al., 2011).

Minimal studies that link diarrhea with intestinal parasites and H pylori have been

undertaken in Kenya while these infections continue to predominate. This study therefore

aims to determine the prevalence of intestinal parasites and H pylori in patients who

presented with or without diarrhea in JOOTRH.

2.2 Intestinal protozoan infections

In India, study done on the spectrum of parasitic infections in patients with diarrhea attending a

tertiary hospital showed that the most common protozoa isolated was Entamoeba histolytica
(37.57%) followed by Giardia lamblia (23.12%), while Entamoeba coli was 23.12%. protozoan

infections were more common than helminthic infections (Saurabh, 2017)

In Mozambique, a study done in Nampula showed that, the prevalence of intestinal parasites in

hospitalized under-five children with diarrhea, estimated that Cryptosporidium spp was the most

common protozoa with a prevalence of 19.9%, while Giardia lamblia 9.7% (Bauhefer et al.,

2021). Using the same diagnostic technique, a rural setting in Manhica district showed higher

frequencies for Crytosporidium spp (18.7%) and G lamblia (17.2%) among children with

diarrhea (Nhampossa et al.,2015) suggesting different geographical distribution for these

protozoa. These protozoa were associated with diarrheal symptoms in the patients.

In Ethiopia, study showed that the prevalence of intestinal protozoan infections among

individuals living with HIV/AIDS was 30.6% (Kiros et al., 2015). Entamoeba histolytica

infection was the most prevalent, followed by Cryptosporidium spp, G lamblia and isospora

belli. In this study diarrhea was found to be more frequent in the patients who were infected with

these parasites.

In Kenya, on the prevalence and genetic diversity of Giardia duodenalis isolates from patients

presenting with diarrhea, showed that diarrhea was commonly caused by the presence of this

protozoa (Mbae et al., 2016). This study presented the first data on the assemblages and sub

assemblages of Giardia duodenalis in children presenting with diarrhea in Kenya.

In Kisumu, little is known on the prevalence of these intestinal protozoan infections which might

be the leading cause of diarrhea. Poor sanitation conditions in the informal settlements of

Kisumu are likely to predispose residents of Kisumu to intestinal parasites which cause diarrhea.

There is paucity of information on intestinal parasites that cause diarrhea in Kisumu. Therefore,
this study seeks to investigate intestinal parasites which cause diarrhea in patients visiting

JOOTRH.

2.2 Intestinal parasitic helminthes

It is estimated that 1.45 billion people are infected with soil transmitted helminthiases in the

world despite all the measures taken to control these infections (WHO, 2020). Infections are

widely distributed in tropical and subtropical areas, with the greatest numbers occurring in sub

Saharan Africa, the Americas, china and East Asia (WHO, 2017).

In Andaman island, study conducted to estimate the prevalence of intestinal parasitic infestation

among pediatric diarrhea patients attending hospitals in Port Blair, showed that Trichuris

trichura was the most prevalent helminthes (9.2%) followed by Ascaris lumbricoides 7.4% and

Strongyloides stercoralis 1.2% (Thamizhmani et al., 2017).

Globally over 600 million people are estimated to be infected by Strongyloides stercoralis and

700 million people live in regions known to be endemic areas, with most of the cases occurring

in sub Saharan Africa (WHO, 2020). In Gabon, study conducted on the intestinal pathogens in

patients with persistent diarrhea that Strongyloides stercoralis had the highest prevalence (10%)

hookworm having 7% and Ascaris lumbricoides 2% (Becker et al., (2017).

In Kenya it is estimated that 6 million people are affected with S. mansomi, with more than 15

million people at risk of infection (WHO, 2017).In Kisumu , a study done to determine the

prevalence and distribution of soil transmitted helminths showed that S.mansomi was the most

prevalent helminth (21%) , S.haemotobium was 3.6%, hook worm 6.1%, A.lumbricoides 4.9%
and T.trichiura 7.7% this high prevalence was as a result of poor sanitation and poor hygiene

practices within Kisumu(Odiero et al 2011). These helminthes are among the leading cause of

diarrhae Kisumu (Rashid et al 2011).

A significant population of Kisumu dwells in informal settlements where exposure to intestinal

helminths is eminent. There is therefore need to identify the helminths associated with diarrhea

in patients at JOOTRH. This study thus seeks to determine intestinal helminths in stool samples

at JOOTRH.

2.3 Helicobacter pylori

H. pylori, initially, had not been recognized as an infectious agent until 1982, in the seminal

work of Nobel Laureates, Warren and Marshall. H. pylori colonizes various regions of the upper

digestive system, mainly the stomach and duodenum, causing stomach and duodenal ulcers and

certain stomach cancers. The infection is today surprisingly common, and the bacteria are

believed to colonize more than half of the world ‘s population (Aziz et al., 2015

Understanding the epidemiological aspects of H. pylori infection is significant and helpful in

illustrating the consequences and complications of the infection. It is also fundamental for the

eradication, treatment, and the establishment of the pattern of antibiotic resistance. Several

Countries in the World Health Organization, Eastern Mediterranean Regional Office (EMRO)

including a group of developing countries in southwest and western Asia as well as North Africa

and the ancient land of Iran, have no systematic reviews on the prevalence and epidemiology of

H. pylori infections (Eshraghian, 2014)

In many countries, the incidence of H. pylori infection has been decreasing steadily in

association with improved standards of living. Yet the occurrence of this bacterium is still ever

present, especially in the Far East (Brown et al., 2002). It is the main cause of chronic gastritis
and the main etiological agent for gastric cancer and peptic ulcer disease (Bauer and Meyer,

2011).

In Brazil, epidemiological studies of H. pylori infection have reported a 40% seroprevalence in

children less than 6 years of age from a low-income population (Camilo et al., 2012). H. pylori

infection is very common among adults in southern Brazil as it is in the other developing

countries. Socio-economic conditions in childhood besides ethnicity and presence of dyspeptic

symptoms in 9 Brazil were found to be the factors significantly associated with the infection

(Santos et al., 2005).

Helicobacter pylori infection is apparent in resource limited countries than in economically

developed countries and the distribution varies between different communities and geographical

locations. About 50% of the population is infected with H. pylori in affluent countries, whereas

this percentage rises to 80% in developing countries, and the prevalence in Ethiopia is in the

range of 48–95% (Shiferaw et al.,2019).

In Kenya, a study conducted on the Prevalence and Endoscopic Findings of Helicobacter

pylori Infection among Dyspeptic Patients in Kenya showed 40.86%.  Gastritis was found to be

the most common endoscopic abnormality among the study population and also among those

who were found to be infected with H. pylori.  However, there was no statistical significance

between gastritis and H. pylori infection (Mwangi et al.,2020)

In Kisumu, little is known on the prevalence of these helicobacter pylori infections which might

be the leading cause of increased gastritis. There is scarcity of information on H pylori that cause

may also be causing diarrhea in Kisumu. Therefore, this study seeks to investigate H pylori

bacteria in patients visiting JOOTRH with abdominal upsets.

3.0 CHAPTER THREE-METHODOLOGY

3.1 study population

The study will involve all patients who will present with or without diarrhea and also those with

gastroduodenal diseases referred to JOOTRH microbiology laboratory for microscopic

examination of parasites and H pylori.

3.2 study site

The current study will be carried out in Jaramogi Oginga Odinga Teaching and Referral Hospital

in Kisumu. Kisumu is Kenya’s third largest county and is located about 400 kilometers

northwest of the capital city, Nairobi. Kisumu county lies within longitudes 33°20'E and latitudes
0°20' south and 0°50'south. The facility is a public hospital operated by the Kenya Ministry of

Health and provides services to the local and outlying communities.

3.3 study design

This will be a cross sectional study investigating the prevalence of intestinal parasites and H

pylori in patients presenting with or without diarrhea who will be referred to microbiology

laboratory at JOOTRH. Stool specimens will be collected and examined for the presence of H

pylori and intestinal parasites.

3.4 sampling

Stratified random sampling will be used; every nth sample referred to parasitology lab will be

examined. The stool samples must be placed in vials within an hour of collection. The stools

will be frozen, not more than 7 days, waiting for examination.

3.5 sample size estimation

The minimum sample size was calculated using the formulae of Fishers et al of 1998 method, using a

prevalence of H. pylori infection of 40% (hospital records).

n=Z 2 P q 2

Where Z score was 1.96 at 95% confidence interval (CI), P was the past prevalence documented (40%),

(hospital records). q was (1 - P), and  was the error at 95% CI which was 0.05.

= [1.96 x 1.96 x 0.4 x (1 – 0.4)]/0.0025

= 368-73

= 295 participants

3.6 inclusion/exclusion criteria

The study will include

 I. all patients who will be presenting with or without diarrhea at JOOTRH and referred to

parasitology lab, who will consent

II. patients who will present with gastroduodenal diseases

III. residents of Kisumu and counties around Kisumu

IV. All ages of patients referred to parasitology lab

The study will exclude

I. patients who will present with other conditions which are not associated H pylori and

intestinal parasites

II. Patients who will not consent

III. Patients who do not reside within the study area

3.7 lab methods

For H pylori

The test will be based on the principle of immunochromatography invitro for qualitative

determination of H. pylori antigens in stool (Bio tracers TM). The test uses H. pylori specific

monoclonal antibodies coated on the membrane of the test device. The cap of the sample

extraction tube will be opened by unscrewing the cap. Using the sample collection stick attached

to the cap, a fresh stool sample, approximately the size of a peanut will be collected from at least

four different sites of the specimen. For liquid or watery stool specimen, 100µl (two drops) of

the sample will be taken using a plastic disposable pipette. The sample collection stick will be

then inserted in to the sample extraction tube containing Phosphate buffer and the tube will be

tightly closed to secure it. The tube will be then swirled and shaken well to dissolve the stool

sample. It will be mixed homogenously with the phosphate buffer in the sample extraction tube

The testing device (cassette) will then be taken out of the foil pouch and paced on a clean and

flat surface, preferably on a bench. Then the dispenser cap of the sample tube will be twisted off

and by holding the tube vertically, five drops of the mixture of the stool sample and buffer will

be dispensed into the sample well of the cassette test device

The stool sample with no antigen (for negative test) will not react with the H. pylori antibody

conjugate in the test device. The buffer and the antibody conjugate will migrate

chromatographically on the membrane of the cassette and no colored line will generate on the

test window. The H. pylori antigen in the stool sample (for positive test) will react with the H.

pylori antibody conjugate in the test device.

For intestinal parasites

The stool specimens will be collected using the modified Ridleys method of stool concentration

(Allen and Ridley ,1970)

Stool examination will be done using both direct and concentration method

Concentration Method

1. 4 mls of 10 formal salines will be measured and poured into a mortal

2. 2 gms of stool will be weighted, placed into a mortal bowl and using a pestle the stool

was thoroughly emulsified

3. The stool emulsion will be sieved through four layers of wet surgical gauze into a

centrifuge tube

4. ¾ mls of ether will be added and a rubber cork placed onto the mouth of the tube

5. The tube will then be shaken thoroughly for twenty seconds

6. The tube contents will be centrifuged at 2000 revolutions per minute for 3minutes and

using applicator stick, the plug of debris will be moved.

7. The supernants will be decanted into the sink, leaving at the bottom a button of stool for

microscopic examinations.

8. Using an applicator stick, the entire button will be carefully dislodged from the tube

buttom and poured directly onto a clean microscope slide.

9. The entire preparation will be examined using 10 or 40 and all the eggs or larvae of the

parasites will be counted.

Direct method
Specimens will be examined as saline iodine wet mounts. the wet mounts fecal preparations will

microscopically be examined under magnification of x400 to detect the presence or absence of

parasites.

3.8 Data analysis

Data will be analyzed using the SPSS version 25.0 software. The prevalence will be determined

and output in bar graphs. Data will be summarized and presented in a descriptive measure such

as table, figures, mean and percent.

3.9 Ethical clearance

Clearance to carry out this research will be sought from the Jaramogi Oginga Odinga Teaching

and Referral Hospital ethical committees with approval from Uzima University department of

microbiology and research. Confidentiality of data and information obtained from this study will

be maintained. Informed consent will be sought from participants. For the participants below the

age of consent; consent will be sought from their guardian. Appropriate treatment will be given

to those

T Proposed budget

MATERIAL COST

Slides 7000

Gauze 1000

Gloves 2000

Reagents. 19000

Stationary 3000

Transport 300

Internet 7000
Printing and binding 7000

Miscellaneous 3000

Approval fee 3000

TOTAL KSH 52,300

WORK PLAN

TASK Jan Feb March April May June July August Sep

2021 202 2021 2021 2021 2021 2021 2021 2021

1
Proposal

Development
Proposal

revision

And approval
lab work

Data collection

and analysis
Presentation of

the findings
Reference

Alwabr, G. M., & Al-Moayed, E. E. (2016). Prevalence of intestinal parasitic infections among

school children of Al-Mahweet Governorate, Yemen. European Journal of Biological

Research, 6(2), 64-73.

Aziz, R. K., Khalifa, M. M., & Sharaf, R. R. (2015). Contaminated water as a source of

Helicobacter pylori infection: A review. Journal of advanced research, 6(4), 539-547.

Bauhofer, A. F. L., Cossa-Moiane, I. L. C., Marques, S. D. A., Guimarães, E. L. A. M., Munlela,

B. A., Anapakala, E. M., ... & de Deus, N. (2021). Intestinal protozoa in hospitalized

under-five children with diarrhoea in Nampula–a cross-sectional analysis in a low-

income setting in northern Mozambique. BMC Infectious Diseases, 21(1), 1-8.

Adamu, H., Endeshaw, T., Teka, T., Kifle, A., & Petros, B. (2006). The prevalence of intestinal

parasites in paediatric diarrhoeal and non-diarrhoeal patients in Addis Ababa hospitals,

with special emphasis on opportunistic parasitic infections and with insight into the

demographic and socio-economic factors. Ethiopian Journal of Health

Development, 20(1), 39-46.

Bizuneh, H., Getnet, F., Meressa, B., Tegene, Y., & Worku, G. (2017). Factors associated with

diarrheal morbidity among under-five children in Jigjiga town, Somali Regional State,

eastern Ethiopia: a cross-sectional study. BMC pediatrics, 17(1), 1-7.

Becker, S. L., Chatigre, J. K., Gohou, J. P., Coulibaly, J. T., Leuppi, R., Polman, K., ... & von

Müller, L. (2015). Combined stool-based multiplex PCR and microscopy for enhanced

pathogen detection in patients with persistent diarrhoea and asymptomatic controls from

Côte d’Ivoire. Clinical microbiology and infection, 21(6), 591-e1.

Brown, L. M., Thomas, T. L., Ma, J. L., Chang, Y. S., You, W. C., Liu, W. D., ... & Gail, M. H.

(2002). Helicobacter pylori infection in rural China: demographic, lifestyle and

environmental factors. International journal of epidemiology, 31(3), 638-645.

Bauer, B., & Meyer, T. F. (2011). The human gastric pathogen Helicobacter pylori and its

association with gastric cancer and ulcer disease. Ulcers, 2011.

Camilo, V., Barros, R., Sousa, S., Magalhães, A. M., Lopes, T., Mário Santos, A., ... & Almeida,

R. (2012). Helicobacter pylori and the BMP pathway regulate CDX2 and SOX2

expression in gastric cells. Carcinogenesis, 33(10), 1985-1992.

Conant, J., & Fadem, P. (2008). A community guide to environmental health. Hesperian

Foundation.
Delahoy, M. J., Omore, R., Ayers, T. L., Schilling, K. A., Blackstock, A. J., Ochieng, J. B., ... &

O'Reilly, C. E. (2018). Clinical, environmental, and behavioral characteristics associated

with Cryptosporidium infection among children with moderate-to-severe diarrhea in rural

western Kenya, 2008–2012: The Global Enteric Multicenter Study (GEMS). PLoS

neglected tropical diseases, 12(7), e0006640.

Eshraghian, A. (2014). Epidemiology of Helicobacter pylori infection among the healthy

population in Iran and countries of the Eastern Mediterranean Region: a systematic

review of prevalence and risk factors. World journal of gastroenterology: WJG, 20(46),

17618.

Gebretsadik, D., Metaferia, Y., Seid, A., Fenta, G. M., & Gedefie, A. (2018). Prevalence of

intestinal parasitic infection among children under 5 years of age at Dessie Referral

Hospital: cross sectional study. BMC research notes, 11(1), 1-6.

Idris, N. S., Dwipoerwantoro, P. G., Kurniawan, A., & Said, M. (2010). Intestinal parasitic

infection of immunocompromised children with diarrhoea: clinical profile and

therapeutic response. The Journal of Infection in Developing Countries, 4(05), 309-317.

Kaakoush, N. O., Castaño-Rodríguez, N., Man, S. M., & Mitchell, H. M. (2015). Is

Campylobacter to esophageal adenocarcinoma as Helicobacter is to gastric

adenocarcinoma?. Trends in microbiology, 23(8), 455-462.

Kiros, H., Nibret, E., Munshea, A., Kerisew, B., & Adal, M. (2015). Prevalence of intestinal

protozoan infections among individuals living with HIV/AIDS at Felegehiwot Referral

Hospital, Bahir Dar, Ethiopia. International journal of infectious diseases, 35, 80-86.

Kiiti, R. W., Omukunda, E. N., & Korir, J. C. (2020). Risk Factors Associated with Helminthic

Intestinal Infection in Lurambi Subcounty, Kakamega, Kenya. Journal of Parasitology

Research, 2020.

Kimang’a, A. N., Revathi, G., Kariuki, S., Sayed, S., & Devani, S. (2010). Helicobacter pylori:

prevalence and antibiotic susceptibility among Kenyans. South African Medical

Journal, 100(1).

La Hoz, R. M., Morris, M. I., & AST Infectious Diseases Community of Practice. (2019).

Intestinal parasites including Cryptosporidium, Cyclospora, Giardia, and Microsporidia,

Entamoeba histolytica, Strongyloides, Schistosomiasis, and Echinococcus: guidelines

from the American society of transplantation infectious diseases community of

practice. Clinical transplantation, 33(9), e13618.

Nhampossa, T., Mandomando, I., Acacio, S., Quintó, L., Vubil, D., Ruiz, J., ... & Alonso, P.

(2015). Diarrheal disease in rural Mozambique: burden, risk factors and etiology of

diarrheal disease among children aged 0–59 months seeking care at health facilities. PloS

one, 10(5), e0119824.

Mohanna, M. A. B., Al-Zubairi, L. M., & Sallam, A. K. (2014). Prevalence of Helicobacter

pylori and parasites in symptomatic children examined for Helicobacter pylori antibodies,

antigens, and parasites in Yemen. Saudi medical journal, 35(11), 1408.

Mesfun, M. G., Fuchs, A., Holtfreter, M. C., Feldt, T., & Häussinger, D. (2019). Causes for

diarrhoea and infection with intestinal parasites among HIV positive patients at a referral

hospital in Central Ethiopia.

Mbae, C. K., Nokes, D. J., Mulinge, E., Nyambura, J., Waruru, A., & Kariuki, S. (2013).

Intestinal parasitic infections in children presenting with diarrhoea in outpatient and

 inpatient settings in an informal settlement of Nairobi, Kenya. BMC Infectious

Diseases, 13(1), 1-11.

Mbae, C., Mulinge, E., Guleid, F., Wainaina, J., Waruru, A., Njiru, Z. K., & Kariuki, S. (2016).

Molecular characterization of Giardia duodenalis in children in Kenya. BMC infectious

diseases, 16(1), 1-7.

Mwangi, C. N., Njoroge, S., Rajula, A., Laving, A., Kamenwa, R., Devani, S., ... & Revathi, G.

(2020). Prevalence and Endoscopic Findings of Helicobacter pylori Infection among

Dyspeptic Patients in Kenya. Open Journal of Medical Microbiology, 10(04), 233.

Odiere, M. R., Opisa, S., Odhiambo, G., Jura, W. G., Ayisi, J. M., Karanja, D. M., & Mwinzi, P.

N. (2011). Geographical distribution of schistosomiasis and soil-transmitted helminths

among school children in informal settlements in Kisumu City, Western

Kenya. Parasitology, 138(12), 1569.

Peterson, K. M. (2008). Strategies for Combating Waterborne Diarrheal Diseases in the

Developing World Investigating Current Appropriate Technologies and their

Effectiveness in Environmental Public Health.

Rashid, M. K., Joshi, M., Joshi, H. S., & Fatemi, K. (2011). Prevalence of Intestinal Parasites

among School Going Children In Bareilly District. National Journal of Integrated

Research in Medicine, 2(1).

Santos, Ina S., Jose Boccio, Ari S. Santos, Neiva CJ Valle, Camila S. Halal, Marta Colvara

Bachilli, and Ricardo D. Lopes. "Prevalence of Helicobacter pylori infection and

associated factors among adults in Southern Brazil: a population-based cross-sectional

study." BMC public health 5, no. 1 (2005): 1-10.

SAID, M. K. (2019). PREVALENCE OF HELICOBACTER PYLORI INFECTION AMONG

PATIENTS WITH PEPTIC ULCERS AND THE ASSOCIATED RISK FACTORS IN

MBAGATHI LEVEL V HOSPITAL, NAIROBI COUNTY, KENYA (Doctoral dissertation,

SCHOOL OF MEDICINE, KENYATTA UNIVERSITY).

Saurabh, K., Nag, V. L., Dash, S., Maurya, A. K., Hada, V., Agrawal, R., ... & Sharma, A.

(2017). Spectrum of parasitic infections in patients with diarrhoea attending a tertiary

care hospital in Western Rajasthan, India. Journal of clinical and diagnostic research:

JCDR, 11(8), DC01.

Schiller, L. R., Pardi, D. S., Spiller, R., Semrad, C. E., Surawicz, C. M., Giannella, R. A., ... &

Sellin, J. H. (2014). Gastro 2013 APDW/WCOG Shanghai working party report: chronic

diarrhea: definition, classification, diagnosis. Journal of gastroenterology and

hepatology, 29(1), 6-25.

Sitotaw, B., Mekuriaw, H., & Damtie, D. (2019). Prevalence of intestinal parasitic infections and

associated risk factors among Jawi primary school children, Jawi town, north-west

Ethiopia. BMC infectious diseases, 19(1), 1-10.

Shiferaw, G., & Abera, D. (2019). Magnitude of Helicobacter pylori and associated risk factors

among symptomatic patients attending at Jasmin internal medicine and pediatrics

specialized private clinic in Addis Ababa city, Ethiopia. BMC infectious diseases, 19(1),

1-6.

Soil Transmitted Helmith Infections.WHO, Fact Sheet Update March; 2016

http://www.who.int/mediacentre/factsheets/fs366/en.
Thamizhmani, R., Sugunan, A. P., Raghvan, P. R., & Vijayachari, P. (2017). Intestinal parasitic

infestation among paediatric diarrhoea patients attending hospitals in Port Blair,

Andaman and Nicobar Islands. Journal of Parasitic Diseases, 41(2), 584-589.

World Health Organization. (2011). Helminth control in school-age children: a guide for

managers of control programmes. World Health Organization.

World Health Organization (2020). Soil transmitted infections WHO World Health Organization

World Health Organization, Diarrheal diseases fact sheet.Geneva,updated 2017.

https://www.who.int/mediacentre/factsheets/fs330/en/