Aklilu et al. BMC Pediatrics(2024) 24:545
https://doi.org/10.1186/s12887-024-05026-0

BMC Pediatrics

RESEARCH

Open Access

Intestinal parasitic co-infections associatedwith Helicobacter pylori among paediatricpatients with gastrointestinal illness attendinga general hospital in southern Ethiopia
Addis Aklilu1* , Melat Woldemariam1*, Edilu Wanke1, Mohammed Seid1, Aseer Manilal1* , Javed Masood Khan2 andIdhayadhulla Akbar3
Abstract
Background Concurrent infections or co-infections caused by intestinal parasites and Helicobacter pylori are quite
rampant in paediatrics living in endemic areas of sub-Saharan Africa, including Ethiopia, and if left untreated, canresult in severe complications and hence must be addressed to ensure their health and well-being.
Objectives To determine the prevalence of intestinal parasitic and H. pylori co-infections and associated factors
among paediatric patients with gastrointestinal symptoms who attended the Arba Minch General Hospital (AMGH),
Arba Minch, southern Ethiopia, from September to November 2020.
Methods A cross-sectional study was conducted among a study population of 299 paediatric patients withgastrointestinal symptoms who visited AMGH. Stool samples were collected and analysed to detect H. pylori andintestinal parasites. A rapid lateral flow chromatographic immunoassay was employed to identify the H. pylori copra
antigen, whereas the latter was detected using wet mount saline preparation and formol-ether concentration
method. Socio-demographic, clinical, behavioural and other factors were obtained by means of a pre-tested
structured questionnaire. Descriptive statistics and logistic regression analysis were done by Statistical Package forSocial Service (SPSS) version 25; P values < 0.05 were considered statistically significant.
Results The prevalence of Helicobacter pylori and intestinal parasites was 14% (n = 42) and 37.1% (n = 111),
respectively, whereas that of the co-infections with these pathogens was 6.4% (n = 19). Giardia lamblia was the mostprevailing parasite, 21.4% (n = 64). Informal maternal education [AOR = 5.14; 95% CI: 1.98–15.70] and lack of handwashing practice were significantly associated with the extent of co-infections [AOR = 4.18; 95% CI: 1.36–12.80].

*Correspondence:
Addis Aklilu
addaklilu@gmail.com
Melat Woldemariamwolde21mealat@gmail.com
Aseer Manilal
aseer.manila@amu.edu.et
Full list of author information is available at the end of the article© The Author(s) 2024. Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0
International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you
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Aklilu et al. BMC Pediatrics(2024) 24:545

Page 2 of 11

Conclusion Nearly one in twenty pediatric patients with gastrointestinal symptoms had intestinal parasitic infectionsand H. pylori co-infections, representing a silent health problem that is to be addressed through effective control
strategies. Health administrators should consider the importance of co-infections in clinical diagnosis and planning
aimed at its prevention.
Keywords Arba Minch, Co-infections, Gastroenteritis, Paediatric patients

Introduction
Helicobacter pylori is a causative agent in gastric andextra-gastric diseases, resulting in significant morbidity
and mortality worldwide [1]. It is one of the most common bacterial pathogens in humans, with an estimated
4.4 billion cases worldwide, including paediatric patients,
and is the fourth leading cause of cancer-related deaths[2]. The global prevalence of H. pylori infection over the
past three decades was 48.9% in adults and 32.3% in children/adolescents, showing substantial heterogeneity [3,4]. The prevalence of H. pylori remains significant amongchildren and adolescents in most of the World HealthOrganization regions [3].
Children can acquire this organism from parents or
peers, leading to the pathogenesis of peptic ulcers, notably duodenal ulcers, and almost all of them with thisdisease have tested positive for the bacterium. Growing quanta of evidence suggests that acquiring an H.
pylori infection in childhood is a significant risk factor
connected to the onset of gastric cancer, such as adenocarcinoma [5]. The incidence and prevalence rates ofchildhood infection with H. pylori vary significantly in
Africa, reflecting the role of various factors like compromised immune system, low socio-economic, educational
status, consumption of contaminated water, as well as
the presence of H. pylori infection existing in the family[6]. Dyspepsia is the illness prevailing among Ethiopians,
including children visiting outpatient departments ofhealth facilities, and it has been reliably correlated with
H. pylori infection [7]. The prevalence of H pylori infection varied considerably across countries and the highest is in the African continent (41.3% in children) [3]. A
systematic review and meta-analysis estimated the overall pooled prevalence of H. pylori infection in Ethiopia
as 52.2% (95% CI: 45.8–58.6) [8]. Gastric cancer is the
13th most common disease and the 10th most common
cause of death in the country [9]. In Ethiopia, the latest
reported prevalence of H. pylori infection in children is
49.3% [3].
The World Health Organization (WHO) has enlisted
parasitic intestinal infections as neglected tropical diseases, and an estimated 3.5 billion (24% of the world
population) globally are afflicted with 450 million casesof symptomatic illness and an annual mortality rate ofover 0.2 million [10]. In Sub-Saharan Africa, it is estimated that up to 250 million are infected with at least any
one species of intestinal parasite [10]. Intestinal parasitic

infections are widespread globally and continue to be theleading cause of human morbidity and mortality, especially in children, due to poor sanitation and hygiene.
As per the report of WHO, soil-transmitted helminthic
infections are the second leading cause of mortality inchildren below six years in the African continent [11].
It is reported that over 267 million preschool-aged children and approximately 568 million school-aged children
live in areas where these parasites are transmitted intensively [12]. A recent systematic review and meta-analysis
reported that the prevalence of intestinal protozoan parasites among African school children was 25.8% [13]. In
Ethiopia, 25.3 million schoolchildren live in situations
where they can contract intestinal parasites easily, andhence, a high probability of H. pylori co-infections exists.
Intestinal parasitic infections are highly prevalent amongchildren, ranging from 66.7 to 83.8% in the country andhave been correlated with adverse outcomes, including
anaemia, malnutrition, stunting, thinness and other mental and physical health problems [14].
The importance of poly-microbial infections has
increased enormously in recent years, and synergistic infections have also been identified; co-infections
involving several species of gastrointestinal parasites arecommonly found in endemic areas of developing countries and are particularly common in young people [15].
The presence of intestinal parasites in children is detrimental, and the consequences include tissue damage,decreased nutrient absorption, malnutrition, or evenimmune deficiency. Colonisation by H. pylori and intestinal parasites is widespread, and it is a fact that theirco-existence mainly occurs in low-income developing
countries, which could be linked pathologically [15]; H.
pylori shares some associated characteristics of intestinal
parasites and has the same transmission route [9]. Bothgroups share similar predisposing factors, including poor
sanitation/hygiene, low socio-economic status, and overcrowding [10]. A previous comprehensive review showedthat co-infections by intestinal parasites and H. pylori canbe correlated to several factors of immunological severe
consequences [16].
In several cross-sectional studies, the pooled prevalence of co-infections with H. pylori and intestinal parasites in different populations was around 11% (95%
Confidence interval: 6.7–17.6%) [17]. A literature scan
indicated that H. pylori and intestinal parasitic coinfections range from 10.6 to 51.4% among the AfricanAklilu et al. BMC Pediatrics(2024) 24:545

population [6, 15, 18–20]. The overall burden was twice
as high in sub-Saharan Africa due to the low economic
status of the region and inferior hygienic practices [6].
In addition, the co-infections with H. pylori in children
were between 23 and 30% in Ethiopia [15, 19]. A closer
look at the literature reveals that co-infections involving H. pylori and intestinal parasites are also endemic
in many regions of the country, but this fact is ignored.
Most of the studies done nationwide in Ethiopia so far
only focused on infections caused by either H. pylori or
intestinal parasites. If the co-infection is not adequately
diagnosed or treated promptly, it can become severe.
One of the primary obstacles in effectively implementing public health measures to address the problems of
co-infections is the inadequacy of comprehensive andcurrent data. Therefore, studies on prevalence and risk
factors associated with co-infections involving intestinal parasites and H. pylori are relevant in the context of
combating the menace in a specific study area. According to AMGH clinical reports, intestinal infections are
currently cited as one of the top reasons for consultation. The present study was designed to determine theprevalence of co-infections by intestinal parasites and H.
pylori, as well as the associated factors existing among
paediatric patients with gastrointestinal illness who were
subjected to stool examination at AMGH.

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Materials and methods
Study design and setting

An institution-based cross-sectional study was conducted at AMGH (Fig. 1) from September 01 to November 30, 2020, which is located in the Gamo Zone [21]. It
currently serves more than 1.5 million annually, providing preventive, rehabilitative, and curative care throughmultiple departments [22]. Approximately 25,000 children receive different healthcare services from this hospital yearly [22]. In addition, there exist a primary hospitaland two health centres in the study area. In total, there
are eight government and eleven private primary schools
in Arba Minch. According to a report on the health anddemographic surveillance system, the total populationof the town is 74,157, of whom 20,062 (27.1%) are aged
between 6 and 14 years [23].
Study population

The study population comprised paediatric patients (lessthan 15 years) with gastrointestinal symptoms and clinically suspected of intestinal parasitic infections, who
attended the outpatient departments of AMGH during
the study period as per the inclusion criteria mentioned
below.

Fig. 1 Map of study area showing the location of study setting, Arba Minch General HospitalAklilu et al. BMC Pediatrics(2024) 24:545

Eligibility criteria
Inclusion criteria

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Outcome variables

Participants selected for the study are aged below 15
years, who attended the outpatient departments during
the above study period, were clinically diagnosed by thephysician based on gastrointestinal complaint and haverequested a stool examination.
Exclusion criteria

The paediatric patients who had received antibiotics andanti-parasitic drugs, proton pump inhibitors, and drugs
containing bismuth compounds four weeks before thecommencement of the study were exempted.
Sample size calculation

The Epi-Info version 7.2 software was used to determine
the sample size using the assumptions of a single population proportion formula. A prevalence of 23% was chosenfrom an earlier study conducted in another part of Ethiopia [15]. After considering a confidence interval of 95%(z = 1.96) and 5% of marginal error (d = 0.05),

n = (Zα/2)2∗ P(1 − P)/d2
n = 3.84 ∗ 0.23(1 − 0.23)/(0.05)2
n = 272

The primary outcome of this study is the prevalence of
co-infections with Helicobacter pylori and intestinal parasites. The secondary outcome includes the identificationof independent factors that influence the co-infections
via analysis.
Independent variables

Independent variables considered in this study include
socio-demographic status, clinical history, and hygiene
related factors mentioned below.
Data collection

A pre-tested structured questionnaire was developed [4,8, 13, 15] and used to accumulate the data. Face-to-faceinterviews with the parents/guardians of each participant
were conducted with the help of well-trained health professionals. Relevant details concerning the socio-demographic status (age, sex, maternal education, occupation,
residence and monthly income), hygiene-related issues(latrine utilisation and hand-washing practices) and clinical factors (intestinal parasitic infections encounteredduring the previous four-month period, history of epigastric pain and treatment measures taken for intestinal parasitic infections) were solicited (Supplementary Table 1).
Specimen collections, transportation and processing

where,
n = required sample size
Zα/2 = Standard normal variant at 5% (P < 0.05) error or
95% confidence interval, 1.96
P = Proportion of co-infected patients from a previous
study
1- P = Proportion of intestinal parasite without coinfections (q)d = Absolute error margin, 0.05
Finally, by computing a 10% non-response rate (i.e., 27
subjects), the sample size was consolidated as 299

The paediatric patients and or guardians were instructed
to place the stool samples directly into a plastic cupwith a tight-fitting lid, following standard collection andtransportation protocols [24]. Participants were also
instructed to wash their hands with soap and water aftercollecting the sample. Approximately 20–40 g of stool
samples were collected into a clean, dry, wide-mouthsterile plastic container labelled with an identification
code and collection date. The stool samples were thentransported to the Medical Microbiology and Parasitology Laboratory of the Department of Medical Laboratory
Science.

Sampling technique

Detection and identification of parasites

A systematic random sampling technique was used toinclude study participants who met the inclusion criteria until the required sample size was reached. The sampling interval was derived by dividing the total numberof target patients by the sample size. The 𝐾th value wasinferred by the N/n formula (N is the number of patients
who visited the hospital in the same period, and n is the
sample size) from which the daily number of patients
who availed the stool examination facilities in the hospital during the study period and was found to be 2. The
first study participant was selected by the lottery method,and subsequently, all 2nd paediatric patients wererecruited into the study.

Stool specimens obtained from all participants were processed without delay. They were examined for the presence of all developmental stages of parasites such as
cysts, oocysts, eggs, trophozoites, larvae and adults bydirect wet mount method using physiological saline anda formol–ether concentration technique as per the WHO
guidelines [24]. Specimens were considered positive even
if one or more helminth eggs, larvae, cysts, or protozoan trophozoites were detected [25]. All examinations
were done twice by two experienced microbiologists,
independently.

Aklilu et al. BMC Pediatrics(2024) 24:545

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Helicobacter pylori Ag determination

Data processing and analysis

The stool samples were tested for the presence of Helicobacter pylori copra antigen by means of a rapid lateral flow chromatographic immunoassay (Guangzhou
Wondfo® Biotech Co., Ltd., Guangzhou, China). Thisqualitative test has a sensitivity of 99.1% and a specificity of 99.2%. The Wondfo One Step H. pylori faeces test
(Cassette) uses a combination of H. pylori antibodies
coated particles and anti-mouse IgG to detect H. pylori
antigens in just a few minutes. Using a sampling stick,stool samples were transferred to a sample collection
tube prefilled with assay diluent solution and mixed wellby gently shaking for a few minutes. Afterwards, 80µL
of sample solution was added to the loading window of
the cassette. After an incubation period of 15 min, theresult was read off in accordance with the manufacturer’s guidelines. The presence of rose-pink bands, both incontrol and test regions, was defined as a positive result,whereas the presence of rose-pink band only in the control region indicates a negative result (i.e., the concentration of H. pylori stool antigens in the sample is below thedetectable level).

The collected data were coded, cleaned, and enteredusing Epi-info version 7.2 and then exported to Statistical Package for the Social Sciences (SPSS) for further
analysis. The IBM SPSS Statistics for Windows, version
25 (IBM Corp., Armonk, N.Y., USA) was used for data
analysis, and descriptive statistics, including frequency,
mean, and standard deviations, were used to describe thestudy participants. The dependent variable in the analysis was co-infections of H. pylori and intestinal parasites.
In order to assess associated factors, a bivariable logistic
regression analysis was done, and to control the probableconfounding effect, only variables with P ≤ 0.25 values in
the former analysis were included in the final model, i.e.,
multivariable logistic regression analysis. The HosmerLemeshow goodness fit test was employed to assess thefitness of the model. The strength of association wasdetermined using adjusted odds ratio (AOR) and 95%
confidence interval (CI), and statistical significance was
assigned only when P values ≤ 0.05.

Data quality assurance

A total of 299 paediatric patients with gastrointestinal
symptoms who met the inclusion criteria took part in
the study with a 100% response rate. The mean age was
8.1 ± 2.5 years; 62.2% (n = 186) were aged between 5 and9 years; there was female preponderance, 52.5% (n = 157)
and 87.3% (n = 261) were urban dwellers. Most of thematernal parents, 80.9% (n = 242), had a formal education, and more than half of them, 51.2% (n = 153), were
homemakers. Details of the socio-demographic data ofparticipants are shown in Table 1. Less than half of thepaediatric patients with gastrointestinal symptoms had
the habit of hand washing (44.8%, n = 134), and 91.3%(n = 273) had the habit of using a latrine. In regard to thehistory of illness, 12% (n = 36) and 28.4% (n = 85) of clients
had experienced parasitic intestinal infections and epigastric pain, respectively (Table 1).

A pre-test of the structured questionnaire was carriedout on 5% of the sample size at the Seikala Health Centre, Arba Minch. Before collecting the actual data andsamples, adequate training was provided to the data collectors and laboratory technicians (who assisted in thesample collection). Data were checked daily for accuracy, clarity, and completeness, and any incompletenessand errors found were immediately rectified. The quality of the H. pylori copra antigen testing kit was assessed
through a quality control test using a known positive
sample, to maintain the quality, standard operating procedures (in-house SOP manual) were followed during collection (aseptic technique), transportation, andprocessing.
Operational definition

Gastrointestinal complaints: Paediatric patients clinicallysuspected of any of the following manifestations (upper
abdominal pain, abdominal bloating, nausea, vomiting,early satiety, heartburn, regurgitation, epigastric pain/
burning, and belching occurring at least thrice a week) by
paediatricians.
Hand washing practices: Washing hands with soap,
always after toileting and before meals.
Co-infections of intestinal parasite and H. pylori: A
positive result for both H. pylori and any intestinal parasitic infection.

Results
Socio-demographic, clinical and hygiene-related factors

Distribution of intestinal parasites, Helicobacter pylori andco-infections

A total of 37.1% (n = 112) of the paediatric patients were
found to be infected with at least any one intestinal parasite. Giardia lamblia was the most commonly isolatedparasite (21.7%, n = 65), followed by E. histolytica / dispar (27%, n = 9). Helicobacter pylori was detected in 14%(n = 42) of the patients. Of the 299 paediatric patients
tested for H. pylori and intestinal parasites, 6.4% (n = 19)
were co-infected (Table 2). The most prevailing co-infections observed were due to the pair H. pylori and G. lamblia (Fig. 2).

Aklilu et al. BMC Pediatrics(2024) 24:545

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Table 1 Socio-demographic, clinical and hygiene-related factorsof paediatric patients with gastrointestinal symptoms
Variable

Category

Frequency

Sex

Male
Female
<5
5–9
10–15
Urban
Rural
Formal education
No formal education
Home
Employee
Merchant
Student< 500
500–1000> 1000
Yes
No
Yes
No
Yes
No

142
157
41
186
72
261
38
242
57
153
63
56
27
22
126
151
134
165
273
26
36
263

Percent
(%)
47.5
52.5
13.7
62.2
24.1
87.3
12.7
80.9
19.1
51.2
18.7
21.1
9
7.4
42.1
50.5
44.8
55.2
91.3
8.7
12
88

85
214
36
263

28.4
71.6
12
88

Age

Residence
Maternal education
Occupation

Household income(Birr)
Hand washingpractice
Latrine utilization

Intestinal parasitic
infections encountered during theprevious four-month
periodHistory of epigastric Yes
pain
No
Treatment measures Yes
taken for intestinal
No
parasitic infections

Table 2 Prevalence of intestinal parasites and Helicobacter pylori
co-infections among paediatric patients
Infection

Category

Frequency

Intestinal protozoan

G. lamblia
E. histolytica
A. lumbricoides
H. nana
T. trichuris
Yes
No
Positive
Negative
Yes
No

65
27
9
7
4
112
187
42
257
19
280

Intestinal helminths

Intestinal parasites
H. pylori antigen test
Co-infections (H.
pylori and intestinal
parasites)

Percent
(%)
21.7
9
3
2.3
1.3
37.4
62.6
14
86
6.4
93.6

Fig. 2 Percentage and diversity of intestinal parasites and Helicobacter pylori co-infections among paediatric patients

Co-infections and associated factors

Bivariable analysis was utilised to examine the association between intestinal parasites and Helicobacter pylori
co-infections and each of the determinant factors. The
results of bivariable logistic regression analysis indicatethat the co-infection was significantly associated withthe sex [P value 0.13, Crude Odds Ratio = 2.54; 95% Confidence Interval: 0.94–6.86], informal maternal education [P value 0.02, COR = 4.35; 95% CI: 1.68–11.28], lackof hand-washing practices [P value 0.06, COR = 2.22;
95% CI: 1.04–7.60], history of infection with intestinal
parasites [P value 0.21, COR = 2.07; 95% CI: 0.04–5.26],
and epigastric pain [P value 0.004, COR = 1.92; 95% CI:
0.20–1.35] (Table 3). However, in the multivariable logistic analysis, only informal maternal education and lack ofhand-washing practices were significantly associated (Pvalue ≤ 0.05) with a higher prevalence of co-infections.
It was observed that paediatric patients having parents
without formal education were found to be five times
more likely to be co-infected than their peers [P value
0.001, Adjusted Odds Ratio = 5.14; 95% CI: 1.98–15.70],
also those without hand-washing practices were 4.1 times
more prone to co-infections than their counterparts [Pvalue 0.011, AOR = 4.18; 95% CI: 1.36–12.80].

Discussions
Gastrointestinal infectious diseases are prevalent indeveloping countries, and Ethiopia is of no exception.
Despite the control measures in place, the magnitude
and impact of Helicobacter pylori and intestinal parasitic infections and co-infection are on the rise. This
study provides some basic information on the individual
prevalence of H. pylori and intestinal parasitic infections

Aklilu et al. BMC Pediatrics(2024) 24:545

Page 7 of 11

Table 3 Bivariable and multivariable logistic regression analyses of associated factors for intestinal parasites and Helicobacter pylori
co-infections among paediatric patients
Variables

Category

Sex
Maternal education
Hand washing practices
Intestinal parasitic infections
encountered during the previous four-month period
History of epigastric pain

COR (95% CI)

P value

AOR (95% CI)

P value

Male
FemaleNo formal education
Formal education
Yes
No
Yes
No

Co-infection
Yes
No
13
129
6
151
9
48
10
232
12
122
7
158
4
32
15
248

2.54(0.94–6.86)
1
4.35(1.68–11.28)
11
2.22(1.04–7.60)
2.07(0.04–5.26)
1

0.13*

2.55(0.92–7.20)
1
5.14(1.98–15.70)
11
4.18(1.36–12.80)
1.26(0.30–5.18)
1

0.07

Yes
No

8
11

1.92(0.20–1.35)
10.004*

1.74(0.13–1.07)
1

0.067

77
203

0.02*

0.06*
0.21*

0.001**

0.011**
0.75*Statistically significant at P ≤ 0.25, ** statistically significant at P ≤ 0.05, AOR: Adjusted odds ratio, COR: Crude odds ratio, 1: reference group, CI: Confidence interval

and also the co-infections prevailing among paediatric patients attending AMGH. Our results revealed that
intestinal parasites and co-infections involving themand H. pylori are growing threats to paediatric patients
attending the study setting.
The prevalence of these parasites varies across regions,even within a country. It is more commonly found inzones and countries characterised by insufficient accessto clean drinking water and inadequate sewage disposal
systems. We found that the rate of H. pylori infection was
14% (n = 42) and was higher than the results (10.4%) ofa study done in Butajira among a group of 6.5-year-old
Ethiopian children [26] and also Lebanon (5.4%) [27]. In
contrast to these, another earlier study conducted in thecapital city of Ethiopia reported a much higher regional
prevalence of 36.8% [28], whereas reports from Nigeria(33.77%) [20], Egypt (42%) [29], and Turkey (29%) [30]
showed some variations in the prevalence. Likewise, acouple of studies done in Butajira, Ethiopia, found that
41 and 44% of 3 and 5-year-old paediatric patients were
infected with H. pylori, respectively [31]. A comparatively
lower prevalence of H. pylori observed in our study could
be explained by the fact that only symptomatic patientswere included.
These observed discrepancies could stem from fluctuations in socio-economic status, environmental exposure, sample size, hygiene practised by participants andother risk factors existing across geographic locations. In
a nutshell, the prevalence observed in our study is lower
than the global average in children (32.6%) [4]. This may
be due to improvements in sanitation, access to quality
water sources, behavioural changes, improved living conditions, increased awareness on the transmission of H.
pylori infection, prompt diagnosis, eradication therapy,
as well as effective prevention and control schemes [8].
Parasitic infection is a more prevalent problem due topoor sanitary conditions, and it affects society dependingon the living conditions of individuals in general, which

include several components such as shoe-wearing habits,
availability of proper restrooms, and other geographic
factors irrespective of the zones or regions. Besides,
socio-environmental factors at the family or community
levels have also been shown to be critical due to the correlation between intestinal parasites and WASH (water,
sanitation, and hygiene) inequalities, parents’ educationlevel, sanitation, and pet health [32].
It is vital to prioritise the routine screening and treatment of parasitic infections in children to prevent complications and to uphold economic productivity andquality of life. The prevalence of intestinal parasites wasfound to be moderate, i.e., 37.4%, highlighting the necessity of immediate intervention and severe planning forprevention. The results of several studies carried out ina similar group of patients in other parts of the country,
such as Ziway (35.7%) [15], Bahir Dar (31.0%) [33], andGondar (34.2%) [34] point towards the urgency of eradication of intestinal parasites. On the other hand, thecondition is considerably better compared to Chencha, asite closer to our study area (81%) [35], Sekota (44.3%),
Ethiopia [36] and also Egypt (58.6%) [29] and Nigeria(75.7%) [37]. A recent systematic review and meta-analysis done in Ethiopia itself showed that the prevalence ofintestinal parasitosis in children of school and preschool
age was 48.0% and the situation is region-specific [38]and is comparatively worse than the scenario existing in
Hawasa (26.6%) [39], Dessie city (16%) [40], and Rama
town (24.4%), Ethiopia [41] as well as Nigeria (21.19%)[20] and Lebanon (6.4%) [27]. Fluctuations observed inour results and those found in previous reports could be
due to differences in the perception of symptoms, levelsof exposure to risk factors selection criteria, method of
diagnosis, study design, and the socio-economic status of
the study population.
In the present study, a total of five species of intestinal parasites were detected in varying percentages.
Out of them, two were protozoans (G. lamblia and E.

Aklilu et al. BMC Pediatrics(2024) 24:545

histolytica), and the remaining were helminths (A. lumbricoides, H. nana, and T. trichuris). As for the protozoan
intestinal flagellate, G. lamblia was the most commonly
isolated, i.e., 21.7% (n = 65). The prevalence and the aetiological agents found by us are identical to those reported
in recent literature. For instance, a similar type of predominance was observed in previous studies conductedin Ziway [15] and Amhara [19] in various proportions. A
study done in Accra, Ghana, also reported the same pattern of predominance [42].
The extent of G. lamblia infection found in our results,
i.e., 21.7%, was similar to that published in a numberof research done in different parts of Ethiopia, such as
Sidama (27.1%) [43], Pawi (26.6%) [44] and Dilla (28%)[45]. However, a systematic and meta-analysis study
revealed that E. histolytica / dispar, followed by Giardia spp., were the most predominant parasites among
schoolchildren in Africa [13]. The second most predominant protozoan found in the current study was the intestinal amoebae, E. histolytica / dispar, i.e., 9% (n = 27), andthis trend resembles the results of a couple of studies performed in Ethiopia [15, 19], even though there are slightvariations in percentages, i.e., between 11.3 (n = 49) − 12.9
(n = 47).
Helminthic infections contribute significantly to gastrointestinal diseases. A meta-analysis study performedon Ethiopian children reported an overall prevalence of
33% (95% CI: 28–38%) [38]. In this study, the tiny intestinal nematode, A. lumbricoides, showed its presence, i.e.,
3% (n = 9), and the same pattern of the predominance of
this nematode in various percentages was reported in astudy done in another part of the country; Amhara, 1.1%
(n = 4) [19]. In the case of A. lumbricoides, a pooled prevalence of 17% (95% CI: 15–19%) was observed in Ethiopian schoolchildren earlier, hinting that one in every
six children in the country lives with Ascariasis [38].
The second most predominant helminth was the intestinal cestode, H. nana, i.e., 2.3% (n = 7), consistent withthe percentage reported in a study conducted in Ziway(n = 10; 2.3%) [15]. A recent meta-analysis done in Southern Nations Nationalities and Peoples Regions provedthat this region of Ethiopia carries the highest burdenof soil helminthiasis and hence can be categorised as aModerate Risk Zone [38]. The prevalence of intestinal
parasitic infections can fluctuate widely due to varying diagnostic criteria, alterations in the characteristics
of clinical populations enrolled, and some mismatching
factors existing among different study populations. The
presence of parasites indicates potential environmental
faecal contamination, likely due to poor hygiene and theabsence of quality water sources, proper sewage systems,
inadequate healthcare, and low levels of public awarenessand education [46].

Page 8 of 11

We found that the prevalence of co-infection was 6.4%,
which was significantly lower than that reported by studies that were carried out among a similar group of participants in several locations in Ethiopia: Ziway (23%) [15]and Amhara (30.8%) [19] and also from Lebanon (11.8%)[27] and a couple of studies from Nigeria [(10.4%) [20]and (14.1%) [47]]. A study done among Egyptian children
also reported a higher co-infection rate (i.e., 43.9%) [18].
The probable reasons for these fluctuations could belinked to the fact that most of the previous studies used aserum antibody test to detect H. pylori, whereas we usedthe copra antigen test. The latter testing method mayunderestimate the extent of consolidation of the prevalence of H. pylori and the rate of co-infections. Above
all, the observed variations in the co-infection rate could
also be attributed to differences in the degree of personal
hygiene practised, socio-economic status, and lifestyle ofthose at risk of infection.
With respect to the combination of organisms associated with co-infections, the majority of H. pylori-positive
patients are infected with the protozoan G. lamblia, too.
A series of studies have reported a higher frequency of
co-infection involving H. pylori and G. lamblia amongchildren [6, 19, 29, 45]. One review article held the viewthat H. pylori could aid the colonisation of intestinal
parasites such as Giardia in the human gastrointestinal
tract by producing urease enzymes, helping to overcome
gastric acidity [18]. Conversely, a parasitic gastrointestinal infection can affect the inflammatory response to
H. pylori [18]. This significant co-existence may indicatethat H. pylori could be a risk factor for parasitic intestinal
infection or vice versa. The co-existence of intestinal parasites and H. pylori could interact synergistically, leading to serious health outcomes that could be influenced
by hosts and environmental factors [18]. These results
suggest that children spend most of their time in highly
contaminated environments, either connected to theirresidences or schools.
In regard to the factors analysed, the educational statusof the maternal parent was significantly associated withthe prevalence of co-infection. Paediatric patients having
mothers with informal education were about five times
more likely to be co-infected. This finding is consistent
with the results of studies conducted in other parts of thecountry [15] and also Lebanon [27]. However, there exists
a sharp contrast in this aspect with respect to previous
studies reported from Ethiopia itself [41] and Ghana [42].
This may be due to the fact that enlightened households
may have an enhanced awareness of the transmissionof infectious diseases and their prevention. Education
brings in changes in healthy behaviours at the household level. Likewise, participants with no hand-washingpractices were significantly associated with co-infections,which agrees with the findings of a meta-analysis carriedAklilu et al. BMC Pediatrics(2024) 24:545

out earlier in the country [13]. Our results indicate thattransmission of co-infection could stem from the fecaloral route, possibly due to inadequate hand hygiene
practices.
The limitations of this work include a cross-sectional
study design with a limited number of participants/sample size, shorter tenure, and the inclusion of only a few
variables. The inclusion and exclusion criteria selection
may also influence the final result to a certain extent.
Serodiagnosis (IgG test), urea breath test or moleculardiagnosis in the case of H. pylori were not done, and due
to a lack of antigen testing facilities, E. histolytica and E.
dispar were not separately identified. Finally, because of
the time constraints experienced during stool collection,
no attempt was made to examine the influence of seasonality with respect to the infection rate.

Conclusion
This study is the first of its kind describing the prevalenceof intestinal parasite infections and Helicobacter pylori,
as well as co-infection rates among paediatric patients
attending AMGH. The results revealed a comparatively
lower prevalence of H. pylori and its co-infections withintestinal parasites in paediatric patients. It was identified that G. lamblia and H. pylori were the most common infections in our study area. Furthermore, informalmaternal education and lack of hand-washing practices
were identified as independent predictors of co-infections. Therefore, large-scale control programs such as
screening, diagnosis, treatment and surveillance, as wellas improved hygiene practices, along with health education, linking the potential sources of infection and transmission of H. pylori and intestinal parasites, are essential
in the study area. Large-scale community-based cohort
studies are imperative to accurately characterise andestablish a cause-and-effect relationship between the risk
factors and co-infection.
Abbreviations
AMGH	Arba Minch General Hospital
AOR	Adjusted odds ratio
COR	Crude odds ratio
CI	Confidence interval
SPSS	Statistical Package for Social ServiceWHO	World Health Organization

Supplementary Information

The online version contains supplementary material available at https://doi.
org/10.1186/s12887-024-05026-0.
Supplementary Material 1
Acknowledgements
The authors acknowledge the support given by the Department of Medical
Laboratory Science, College of Medicine and Health Sciences, Arba Minch
University, in the form of a facility. Thanks are extended to all the study
participants/guardians who were involved in this research. The authors are

Page 9 of 11

also thankful to the Researchers Supporting Project number (RSP2024 R360),King Saud University, Riyadh, Saudi Arabia. Thanks are extended to Prof. Dr.
Sabu for the critical English language.
Author contributions
Conceptualization-AA, MW, MS, AM, EW. Methodology-AA, MW, MS, AM, EW,
JM, IA. Software-AA, MW, AM. Investigation-EW, AA, MW, MS, AM. Formal
analysis-AA, MW, AM, MS, JM, IA. Writing - Original Draft-AA, MW, AM. Writing Review & Editing- AA, MW, AM, JA, IA.
Funding
This research received no specific grant from any funding agency.
Data availability
The data sets generated during and/or analyzed during the current study areavailable from the corresponding authors upon reasonable request.

Declarations
Ethics approval and consent to participate
Ethical clearance was given by the Institutional Research Ethics Review
Board, College of Medicine and Health Sciences, Arba Minch University (Ref.
AMU/9/31/43). This study was conducted in accordance with the Declarationof Helsinki.A signed-up (written) informed consent was obtained from theparents/guardians of each paediatric patient. In addition, assents werealso obtained from older paediatric patients (12 to 15 years) before thecommencement of the actual collection of data and samples. Participants
were guaranteed the right to withdraw from the study by declining thesubmission of their stool samples, without affecting the medical aid/services
received by them. All samples were coded to ensure the confidentiality ofparticipants’ personal information. Finally, results were communicated to their
paediatricians and recorded on the medical card of the respective patient.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Author details
1
Department of Medical Laboratory Science, College of Medicine and
Health Sciences, Arba Minch University, Arba Minch, Ethiopia
2
Department of Food Science and Nutrition, College of Food andAgricultural Sciences, King Saud University, Riyadh 11451, Saudi Arabia
3
Research Department of Chemistry, Nehru Memorial College (Affiliatedto Bharathidasan University), Puthanampatti, Tamil Nadu 621007, India
Received: 16 May 2024 / Accepted: 19 August 2024

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