Effect of Intestine Parasite Infection on Stunting in Children: A

Meta-Analysis Study

Hanna Mutiara

1,2

, Agnes Kurniawan

and Lisawati Susanto

Section of Microbiology and Parasitology, Faculty of Medicine, University of Lampung, Indonesia

FKUI Clinical Parasitology Specialist Doctoral Education Study Programs, Indonesia

Keywords: Intestinal Worms, Intestinal Parasitic Infections, Meta-Analysis, Intestinal Protozoa, Stunting.

Abstract: Stunting is a child health problem that describes a chronic nutritional problem. One of the causes of stunting

is intestinal parasitic infection. Research related to the risk factors for stunting has been widely carried out,

but related to intestinal parasite infection as one of the determinants is still limited and still being debated.

Therefore, it is necessary to make a meta-analysis study. Search for published and unpublished articles

according to the flow on the Prisma diagram online through PubMed, Science Direct, Google Scholar,

Hindawi, Cochrane library, DOAJ, JSTOR, Public Library of Science (PLoS), UI repository, Unila and USU

in a timeframe 2016 to 2021 with Indonesian and English versions. The keywords used were intestinal

parasitic infection, soil transmitted helminth infection, intestinal protozoan, stunting, growth disorders,

children, intestinal parasitic infections, intestinal protozoa, short stature and children. The article search was

carried out using keywords and Mesh terminology using the Quatation mark "", the boolean operators "OR"

and "AND". The search results obtained 1042 journals and 2 theses. Then, screening and review were carried

out to obtain 6 suitable journals to be analyzed using review manager 5.4 software. The combined p-value of

the meta-analysis results was p=0.02 with an OR of 1.48 (95% CI 1.06-2.07). This means that there is an

effect of intestinal parasitic infection on the incidence of stunting in children.

1 INTRODUCTION

Stunting is a child health problem, not only in the

world, but also in Indonesia. In 2015, around 23.2%

or 159 million children under five experienced

stunting (Shekar, 2017). Data from 2017 shows that

55% of children under five are stunted in the world

originate from Asia and 39% live in Africa. The order

of proportion of stunted children under five in Asia is

South Asia (58.7%), Southeast Asia (14.9%), East

Asia (4.8%), West Asia (4.2%) and Central Asia

(0.9%). According to data from the World Health

Organization (WHO), the prevalence of stunted

toddlers in Indonesia in 2005-2017 was the third

highest in the Southeast Asia region or South-East

Asia Regional (SEAR), namely 36.4% (Ministry of

Health of the Republic of Indonesia, 2018; UNICEF,

2020).

Based on Nutrition Status Monitoring (PSG) data,

the highest prevalence of nutritional problems in

Indonesia is stunting, namely 27.5% in 2016 and

29.6% in 2017, while Basic Health Research

(Riskesdas) in 2018 produced prevalence data of

30.8% (Ministry of Health of the Republic of

Indonesia, 2018). Nutritional problems do not only

occur in toddlers, but also in children and adolescents.

Nationally, the prevalence of stunting in children

aged 5-12 years is 23.6% and in adolescents aged 13-

15 years is 25.7% (Ministry of Health of the Republic

of Indonesia, 2018).Handling stunting has been

designated as one of the priority programs (Ministry

of Health of the Republic of Indonesia, 2018; CPM,

2020).

Stunting is divided into two categories, namely

short with a Z score threshold of -3.0 to -2.0 standard

deviation (SD) and very short with a Z score threshold

of less than -3.0 SD (Ministry of Health of the

Republic of Indonesia, 2020; Harjatmo, 2017).

Stunting has serious impacts both in the short and

long term, including increasing child morbidity and

mortality. The incidence of stunting at an early age

can continue and there is a risk of short growth in

adolescence. Therefore, interventions to prevent

stunting growth are still needed even after exceeding

the First 1000 Days of Life (HPK) (Ministry of Health

of the Republic of Indonesia, 2018; Aryastami, 2017).

182

Mutiara, H., Kurniawan, A. and Susanto, L.

Effect of Intestine Parasite Infection on Stunting in Children: A Meta-Analysis Study.

DOI: 10.5220/0013667900003873

Paper published under CC license (CC BY-NC-ND 4.0)

In Proceedings of the 1st International Conference on Medical Science and Health (ICOMESH 2023), pages 182-194

ISBN: 978-989-758-740-5

The causes of stunting consist of several factors,

namely basic causes, underlying causes and

immediate causes. Basic causes are adequate

household quality support (such as housing,

education, work, income and technology), socio-

cultural, economic and political conditions.

Underlying causes include household food security

conditions, parenting patterns, sanitation and health

of the household environment, and health services.

Immediate causes include food intake and infectious

diseases.

One of the infectious diseases is caused by

intestinal parasites which often affect children,

especially in tropical areas such as Indonesia

(Ministry of Health of the Republic of Indonesia,

2018; Aryastami, 2017; Torlesse, 2016; Setiawan,

2018).

Intestinal parasitic infections can be caused by

intestinal protozoa and intestinal worms. The

intestinal protozoa that are often found are Giardia

lamblia, Blastocystis hominis, Entamoeba and

Cryptosporidium. The prevalence of intestinal

protozoan infections is still relatively high. Research

in Ethiopia on 500 children aged 1 to 5 years found a

prevalence of intestinal parasitic infections of 47%

and the highest was Giardia lamblia infection (22 %)

(Osman, 2020). Children with giardiasis are 3.5 times

more likely to be malnourished than those without

Giardia lamblia infection (Osman, 2020). Likewise,

in Mexico, 34% of children aged 6 months to 5 years

were infected with intestinal parasites, namely

Ascaris lumbricoides, Entamoeba histolytica and

Giardia lamblia (Gutiérrez-Jiménez, 2019). Research

in Bekasi, West Java, Indonesia also provided data on

the prevalence of Blastocystis hominis at 60.8%,

Giardia lamblia at 33.8% and Entamoeba histolytica

at 1.4% (Winita, 2016).

Intestinal protozoal infections are generally

water-borne diseases that are transmitted via the oral-

fecal route (Mahardianti, 2020). Transmission can

occur easily, especially in areas with low sanitation

and hygiene conditions. This causes high morbidity

rates which of course affect the sufferer's quality of

life. Manifestations of this disease can include

nausea, vomiting, abdominal pain and diarrhea

(Pramestuti, 2017). Intestinal protozoal infections can

cause problems with digestion and absorption of

nutrients. This is partly due to shortening and

dystrophy of the intestinal microvillus or the

formation of ulcers (Herbowo, 2016).

Intestinal worm infections are most often caused

by soil transmitted helminth (STH) worm parasites.

Ascaris lumbricoides, Trichuris trichiura, and hook

worms ( Necator americanus and Ancylostoma

duodenale ) are nematodes that include STH

(Jourdan, 2018; Sutanto, 2008). Intestinal worm

infections generally are chronic and asymptomatic.

This parasite can affect the intake, digestion,

absorption and metabolism of food in the host's body.

The World Health Organization estimates that

worldwide STH infection sufferers are more than 1.5

billion people (24%). More than 600 million school-

age children and 270 million preschool-age children

live in areas with intensive parasite transition and are

therefore at high risk of infection (WHO, 2020). In

500 children aged under 5 years in Ethiopia, 15%

were infected with Ascaris lumbricoides (Osman,

2020). The prevalence in Indonesia varies, but is still

in the high range. Research conducted by Mutiara in

2014 at several state elementary schools in one sub-

district in the West Java region, found that the

prevalence of STH infection was 23.2% (Mutiara,

2014). Meanwhile, the prevalence in one of the state

elementary schools located in South Lampung

Regency was 43.1%. This infection is included in

neglected tropical diseases (NTDs) so attention

regarding its management, including management

and elimination efforts, is not yet optimal.

Research regarding risk factors for

stunting has

been widely carried out, however regarding intestinal

parasitic infections as one of the determinants is still

limited and still debated (Hailegebriel, 2018; Yoseph,

2020). In addition, treating intestinal parasitic

infections has not been a priority in implementing

stunting management programs in Indonesia.

Therefore, it is necessary to carry out systematic

reviews and meta-analysis research to synthesize data

related to the influence of intestinal parasite

infections on stunting in children.

2 THEORETICAL REVIEW

2.1 Child Nutritional Status

Stunting is a child health problem, not only in the

world, but also in Indonesia. Stunting is nutritional

status based on body length (PB) or body height (TB)

index according to age. This indicator provides an

indication of chronic nutritional problems. Another

anthropometric indicator for assessing the nutritional

status of toddlers is weight for height (WW/TB),

which provides an indication of acute nutritional

problems. The BB/TB and BMI/U indicators can be

used to identify thin and fat. The problem of being

thin and fat at an early age can result in the risk of

various degenerative diseases in adulthood (Ministry

of Health of the Republic of Indonesia, 2018).

Anthropometry is the measurement of the human

Effect of Intestine Parasite Infection on Stunting in Children: A Meta-Analysis Study

183

body, while nutritional anthropometry relates to

various measurements of body dimensions and body

composition as well as age and nutritional levels. The

nutritional status assessment categories are presented

in table 1.

In growth there are 4 interrelated periods, namely

fetus, infancy, childhood and puberty. Age 6 to 24

months determines linear growth. Inadequate

nutrition can cause irreversible damage and lead to

impaired physical and cognitive growth. The first

thousand days have been declared a critical period for

nutritional interventions and addressing problems

that interfere with nutritional adequacy (Budge,

2019). The combined effects and interactions of

infection, environmental and dietary factors as

determinants of stunting in children have long been

considered very important.

Table 1: Categories and Thresholds for Children's Nutritional Status Based on Index (Minister of Health of the Republic of

Indonesia, 2020)

Index Nutritional Status Category Threshold (Z-score)

Body weight according to age (WW/U)

Children aged 0-60 months

Extremely underweight <-3 SD

Underweight -3 SD to <-2 SD

Normal weight -2 SD to +1 SD

Risk of being overweight > +1 SD

Body length according to age (PB/U) or

Height according to age (TB/U)

Children aged 0-60 months

Very Short (severely stunted) <-3 SD

Short (stunted) -3 SD to <-2 SD

Normal -2 SD to +3 SD

Tall > +3 SD

Body weight according to body length

(BB/WW) or according to height

(WW/TB)

Children aged 0-60 months

Malnutrition (severely wasted) <-3 SD

Malnutrition (wasted) -3 SD to <-2 SD

Good (normal) nutrition -2 SD to +1 SD

Risk of overnutrition (possible

risk o

overwei

ht)

> +1 SD to +2 SD

Over nutrition (overweight) > +2 SD to +3 SD

Obesity (obese) > +3 SD

Body mass index according to age

(BMI/U)

Children aged 0-60 months

Malnutrition (severely wasted) <-3 SD

Malnutrition (wasted) -3 SD to <-2 SD

Good (normal) nutrition -2 SD to +1 SD

Risk of overnutrition (possible

risk o

overwei

ht)

> +1 SD to +2 SD

Over nutrition (overweight) > +2 SD to +3 SD

Obesity (obese) > +3 SD

Body mass index according to age

(BMI/U)

Children aged 5-18 years

Malnutrition (severe thinness) <-3 SD

Malnutrition (thinness) -3 SD to <-2 SD

Good (normal) nutrition -2 SD to +1 SD

Over nutrition (overweight) +1SD to +2 SD

Obesity (obese) > +2 SD

ICOMESH 2023 - INTERNATIONAL CONFERENCE ON MEDICAL SCIENCE AND HEALTH

184

Diarrhea or parasitic infections are infections that

occur frequently and repeatedly and are associated

with an increased risk of stunting (Milward, 2017).

Exposure to pathogens can cause disruption of

intestinal structure and function. This condition is

known as environmental enteric dysfunction (EED)

which is characterized by villous atrophy of intestinal

mucosal cells, crypt hyperplasia, increased

permeability, and inflammatory cell infiltration. This

EED condition can result in disruption of the

intestinal immune response, reducing the delivery,

absorption and utilization of nutrients resulting in a

state of nutritional deficiency (Budge, 2019; Dewey,

2011).

2.2 Intestinal Parasitic Infections

Soil transmitted helminthiasis is an intestinal worm

infection that often occurs in children in tropical

areas, including Indonesia, especially in areas with

poor sanitation. This group of intestinal worms

requires moist and warm soil as a medium for the egg

stage to develop into an infective stage, either

infective eggs or infective larvae. Intestinal worms

included in this group are Ascaris lumbricoides,

Trichuris trichiura and hook worms (Ancylostoma

duodenale and Necator americanus) (Hadidjaja,

2011).

Protozoa are eukaryotic unicellular

microorganisms that resemble animals, are

heterotrophs and live as parasites in the bodies of

other organisms. Protozoa can survive in a free

environment by forming cysts, and in the body other

organisms move using means of movement in the

form of pseupodia, cilia and flagella. Protozoa is a

subdivision that comes from Kingdom Protista.

Based on movement or locomotion, the Protozoa

subdivision is divided into 4 phyla, namely

Sarcomastigophora, Ciliophora, Apicomplexa, and

Microspora. Protozoa can infect the intestines, blood,

lung tissue and other extraintestinal tissues. The

species of intestinal protozoa in hosts (humans),

especially in children, that are often found include

Entamoeba sp, Giardia sp, Blastocystis sp,

Balantidium sp, and Cryptosporidium sp.

Laboratory examination is an important aspect in

diagnosing parasitic diseases. Placing fixation labels,

use of special containers, where specimens are

collected and how they are disposed of need to be

considered. Fresh feces specimens are collected in a

clean container, with a wide mouth and a tight lid to

prevent spillage and maintain humidity. Stool

specimens should not be mixed with water and/or

urine. Each specimen sent to the laboratory must be

accompanied by the patient's name, identification

number, name of the doctor or specimen sender, date

and time of specimen collection. The specimen must

also be accompanied by a request form for the type of

laboratory examination requested. It is better if

accompanied by information about possible

diagnoses or certain characteristics, such as travel

history (Hadidjaja, 2011; Garcia, 2016).

To examine parasites in feces, it is recommended

to collect three specimens sent on different days or

one day apart but not more than 10 days apart. Two

specimens were collected after normal defecation

while another specimen was collected after laxative

administration. If you suspect intestinal amoebiasis

infection, six specimens should be taken. Liquid stool

specimens should be examined within 30 minutes of

the stool being passed while soft stools should be

examined within 1 hour. If this is not possible, then

the specimen must be given a preservative. Solid

stool specimens may be examined at any time within

24 hours of the stool being passed. Preservatives that

can be used include formalin, merthiolate

(thimerosal) iodine formalin (MIF), sodium acetate-

acetic acid-formalin (SAF), Schaudinn's solution and

polyvinyl alcohol (PVA) (Garcia, 2016).

Specimen delivery must be carried out using a

double container. The inner container is an aluminum

cylinder with a screw cap which is then wrapped in

cotton to maintain moisture and absorb materials that

may escape due to leaks. Next, the container is placed

in an outer container made of cardboard.

Intestinal parasite examination methods that can

be used are direct preparation, concentration method

and removal preparation with permanent smear.

Direct preparations were made by mixing about 2 mg

of feces with a drop of 0.85% salt solution, then

covered with a 22x22 mm glass cover. The entire

surface of the cover glass was examined

systematically using 100x magnification and low

light intensity then with medium magnification

(400x). The concentration method is part of the

routine parasite examination procedure to detect

parasites that may not be found in a direct preparation

examination. There are two types of concentration

procedures, namely flotation and sedimentation. This

method is designed to separate protozoa and worm

eggs from feces through differences in specific

gravity. Permanent smear preparations not only allow

the examiner to store the preparation permanently,

but can also be used for further consultations. This

preparation is recommended for every stool sample

examination. There are several smear techniques,

namely the Heidenhain method of iron hematoxylin,

trichrome or modified iron hematoxylin.

Effect of Intestine Parasite Infection on Stunting in Children: A Meta-Analysis Study

185

In providing therapy for intestinal worm

infections, especially STH, in children over 2 years,

WHO recommends albendazole 400 mg and

mebendazole 500 mg given as a single dose orally.

For children aged 1 year to 2 years, the dose of

Albendazole that can be given is 200 mg. However, it

seems that these therapy guidelines need to be

updated considering the large number of studies

regarding this anthelmintic regimen. It is now known

that benzimidazole drugs have limitations, namely

their low efficacy against Trichuris trichiura and

hookworms, as well as the emergence of the risk of

resistance. So now multiple drug therapy appears to

be a potential solution.

Moser's research on the combination of

anthelmintics for hookworm infections showed that

the administration of a three-drug regimen

(albendazole 400mg, pyrantel pamoate 20mg/kgBB,

and oxantel pamoat 20mg/kgBB) had the highest cure

rate (84.1%) compared to administration of

albendazole and oxantel pamoate or administering

pyrantel pamoate and oxantel pamoate at the same

dose. Studies in the Philippines also showed that

ivermectin plus albendazole had higher efficacy

against T. trichiura infections than monotherapy.

Other studies have also shown the benefit of dual drug

therapy including administration of oxantel and

tribendimidine in the treatment of infections with T.

trichiura and other STH species (Brooker, 2018;

Eshetu, 2020).

Therapy for intestinal protozoal infections

consists of several options. In Giardia lamblia

infection, metronidazole is an effective treatment.

Until 2002, treatment for cryptosporidiosis was

unsatisfactory, but now it has shown improvement.

Of the many drugs screened for having

anticryptosporidial activity, it is known that

paromomycin and nitazoxanide show clinical

improvement in patients (Farthing, 2006). In the

treatment of amoebic colitis, nitroimidazole

derivatives are the drugs of choice because they are

very effective in treating the trophozoite form.

Metronidazole can be given at a dose of 750-800 mg,

three times a day for 5-10 days, or tinidazole at a dose

of 2 g every day for 3 days. However, this drug has

little effect on amoebic cysts so it is recommended

that treatment be followed by administration of

paromomycin or diloxanide furoate which work on

organisms in the lumen (Farthing, 2006). These

procedures are summarized in table 2.

Table 2: Therapy for Diarrhea Caused by Protozoa (Farthing, 2006)

Intestinal Protozoa Therapy Alternative therapy

Giardia lamblia Metronidazole 1 g/dose for 3 days Tinidazole 2 g single dose

Cryptosporidium parvum

Nitazoxanide 500 mg twice daily for 3–

14 days

Albendazole 400 mg twice daily for 7–

14 days

Paromomycin 500 mg four times a day

for 7

–

14 days

Cyclospora cayetanensis

Co-trimoxazole (trimethoprim 160 mg

and sulfamethoxazole 800 mg) twice

daily for 7 days

Ciprofloxacin 500 mg twice daily for 7

days

Isospora belli

Co-trimoxazole (trimethoprim 160 mg

and sulfamethoxazole 800 mg) mg four

times a da

for 10 da

Ciprofloxacin 500 mg twice a day for 7

days

Entamoeba histolytica

Metronidazole 750 mg three times a day

for 5 days

Diloxanide furoate 500 mg three times a

day for 10 days

Paromomycin 25-35 mg/kgBB three

times a day for 7-10 days

Balantidium coli

Metronidazole 400 mg three times a day

for 10 days

Tetracycline 500 mg four times a day for

10 days

Blastocystis hominis

Nitazoxanide 500 mg twice a day for 3

days

Metronidazole 800 mg three times a day

for 5-10 days

Co-trimoxazole (trimethoprim 160 mg

and sulfamethoxazole 800 mg) twice a

day for 7 days

Encephalitozoon intestinalis Albendazole 400 mg twice a day for 14-

28 days

Not yet available

Enterocytozoon bieneusi

Albendazole 400 mg twice a day for 28

days

Fumagillin 60 mg daily for 14 days

ICOMESH 2023 - INTERNATIONAL CONFERENCE ON MEDICAL SCIENCE AND HEALTH

186

3 METHODS

The research was conducted in June 2021 – July

2021. Data or literature collection was carried out

through electronic media, namely in the form of

published and unpublished results of primary

research regarding intestinal parasitic infections on

the incidence of stunting in children. Literature

searches via electronic media were carried out online

via the Unila, UI and USU repositories, as well as via

PubMed, Science Direct, Google Scholar, Hindawi,

Cochrane library, DOAJ, JSTOR, Public Library of

Science (PLoS). Some of the keywords used are

intestinal parasitic infection, soil transmitted

helminth infection, intestinal protozoan, stunting,

growth disorders, and children. Key words used in

searching through the repository were intestinal

parasitic infections, soil transmitted helminths,

intestinal protozoa, short stature, stunting and

children.

4 RESULT

Article searches were carried out using keywords and

Mesh terminology for each PICO component using

the Quatation mark "", Boolean operators "OR" and

"AND". The results of searching all sources using

keywords obtained 1042 journals and 2 theses.

Articles that experienced duplication were deleted

and then filtered based on the title and 182 suitable

journals were obtained. Then verification was carried

out through abstracts that met the inclusion criteria

and 21 suitable journals were obtained. Then content

verification was carried out and 9 appropriate

journals were obtained. Then an in-depth review was

carried out and it was found that 3 studies were not

relevant because the research data was prevalence

data and compared data between regions, not between

variables, so they did not meet the inclusion criteria.

Therefore, 6 articles were obtained that could be

analyzed in the meta-analysis. A description of the

research search results is presented in Figure 1.

Figure 1. PRISMA diagram of article selection flow

Literature searching (n = 1044)

Published (n = 1042) Unpublished (n = 2)

PubMed: 59 Repository UI: 0

Google Scholar: 655 Repository Unila: 1

Cochrane Library: 16 Repository USU: 1

DOAJ: 0

Hindawi: 5

Science Direct: 293

PLOS: 3

JSTOR: 11

Title’s reviewed:

Unrelevan studies (n= 858)

Double article (n=4)

Title

(

n = 182

)

Abstract’s reviewed:

Unrelevan studies (n= 161)

Abstract (n=21)

Full article (n=9)

Full article’s reviewed:

Not open access (n=4)

Unrelevan studies (n= 8)

Unrelevan dependent’s variable

Studies analysis (n=6)

Unrelevan studies 3 because:

Unrelevant data (only prevalence)

Effect of Intestine Parasite Infection on Stunting in Children: A Meta-Analysis Study

187

Data analysis was carried out using review

manager 5.4 software. Selected articles were

published by PLOS, BioMed Central Public Health

(BMC), Sage Open medicine, and Journal of

Epidemiology and Public Health (JEPH). The

research was conducted in Nangapanda District,

Indonesia, Southern Ethiopia, Bahir Dar Ethiopia,

Southwest Ethiopia, and Pinrang District, South

Sulawesi, Indonesia. All subjects analyzed were 5,687

children aged 6 months to 18 years. The entire study

used a cross sectional design. The characteristics of

the research data in the article are presented in table 3.

Table 3. Characteristics of Research Data

ource Type Year

publi-

cation

Writer Title Loca-

tion

n Sub-

ject's

age

Inspection Prevalence aOR 95%CI

Stun-

ting

Para-

site

Stun-

ting

Para-

site

PLOS

ournal

2021 Djuardi

Soil-

transmitted

helminth

infection,

anemia, and

malnutrition

among

preschool-

age children

Nangapand

subdistrict,

ndonesia

Indo-

nesia

393

1-5

yrs

HAZ

score

Kato

Katz

Metho

40.2%

58.8% 1.23

0.63-

2.39

PLOS

ournal

2017 Grimes

Sanitation,

hookworm,

anemia,

stunting,

and wasting

in primary

school

children in

southern

Ethiopia:

Baseline

results from

a study in 30

chools

Ethiop

3686

5-18

yrs

HAZ

score

Kato

Katz

Metho

28% 23% 0.99

0.79-

1.25

BMC

ournal

2018 Hailege

briel

Undernutriti

on,

intestinal

parasitic

infection

and

associated

risk factors

among

selected

primary

school

children in

Bahir Dar,

Ethiopia

Ethiop

382

7-13

yrs

HAZ

score

Forma

lin-

Ether

concen

tration

metho

18.3% 52.4% 1.1 0.65-

1.86

AGE

ournal

2020 Mekonn

Soil-

transmitted

helminth

infections

and

nutritional

status of

school

children in

overnment

Ethiop

404

6-14

yrs

HAZ

score

Direct

wet

mount

and

McMa

ster

metho

21% 55% 2 1.2-

3.33

ICOMESH 2023 - INTERNATIONAL CONFERENCE ON MEDICAL SCIENCE AND HEALTH

188

elementary

schools in

Jimma

Town,

Southwester

n Ethiopia

JEPH

ournal

2020 Muslim

Multilevel

Analysis

Association

of Soil

Transmitted

Helminths

and Stunting

in Children

Aged 6-12

Years Old in

Pinrang

District,

South

Sulawesi

Indone

sia

200

6-12

yrs

HAZ

score

Stool

exami

nation

(not

explai

ned

further

)

46.5% 41% 2.11 1.11-

4.01

BMC

ournal

2020 Joseph The high

prevalence

of intestinal

parasitic

infections is

associated

with

stunting

among

children

aged 6–59

months in

Boricha

Woreda,

Southern

Ethiopia: a

cross-

sectional

tudy

Ethiop

622 6

mont

hs-5

years

HAZ

score

Direct

wet

mount

and

Kato

Katz

metho

39.3% 48.7% 2.18 1.36-

3.49

Note: HAZ = Height-for-age-z-score with classification based on WHO guidelines

Analysis of variations between studies is aimed at

determining whether the studies are heterogeneous or

homogeneous. Between studies it is said to be

homogeneous if the p value in the heterogeneity test

is greater than 0.05 or the intuitive index (I

) and Tau

values are small. The results of the analysis show that

of this analysis is 67%, meaning that the variation

between studies is heterogeneous, so the model used

to calculate the combined effect is the random effect

model.

Figure 2. Forest Plot Random Effect Model.

Effect of Intestine Parasite Infection on Stunting in Children: A Meta-Analysis Study

189

The forest plot shows the odds ratio for each study

with its confidence interval (horizontal line). The

combined odds ratio is depicted in a diamond shape

(black). The combined effect value from the results of

the analysis of these six studies was 1.48 with a 95%

confidence interval of 1.06-2.07. The combined

effect also produces a Z value of 2.27 and a p value

of 0.02. This means that there is an influence between

intestinal parasitic infections on the incidence of

stunting in children. Children with intestinal parasitic

infections are 2.27 times more stunted than children

without intestinal parasitic infections.

Funnel plots can be used to determine research

variation and publication bias. If the number of plots

on the left and right sides is balanced and the distance

between plots is balanced, it means there is no

publication bias. This means that if the analysis is

carried out on different populations, times, places and

conditions, the results will remain consistent. The

results of this meta-analysis show a balanced funnel

plot.

Table 4. Effect size of combined studies

Model

Effect Size and 95%CI Si

nificance test

Number of Research Combined Effects Lower limit Upper limit Z p

Rando

6 1.48 1.06 2.07 2.27 0.02

Figure 3. Funnel Plot

5 DISCUSSION

Many studies have been conducted regarding

intestinal parasitic infections and stunting, but have

produced varying results. Therefore, statistical

analysis was carried out using meta-analysis to prove

the quality of each research so that new quantitative

data could be obtained and more accurate conclusions

could be drawn.

These six studies were analyzed involving 5,687

research subjects and the combined effect results

concluded that there was an influence between

intestinal parasitic infections on the incidence of

stunting in children with an OR of 1.48 (CI 95%:

1.06-2.07). In determining stunting status, all

researchers used the same method, namely based on

height-for-age-z-score which was then classified

according to WHO guidelines. Intestinal parasite

examination is carried out using stool specimens and

then examined in the laboratory. Examination

methods in general are direct wet mount and the Kato

Katz method, except for the Hailegebriel study which

used the Formalin-Ether concentration method and

Mekonnen used the McMaster method (Hailegebriel,

2018; Yoseph, 2020; Mekonnen, 2020; Grim, 2017).

In research in Nangapanda, there were 58.8% of

intestinal parasitic infections which were

predominantly caused by Ascaris lumbricoides

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(47.4%) followed by Trichuris trichiura (36.8%) and

hookworm (9.2%). A total of 28.7% of subjects

experienced multiple infections, namely 20.6%

coinfected with Ascaris lumbricoides with Trichuris

trichiura, 2.2% coinfected with Ascaris lumbricoides

with hookworm and 5.9% coinfected with the three

species. A single parasitic infection has been proven

to be related to the incidence of stunting. The same

thing with moderate intensity infections. However,

this is not the case with multiple parasitic infections,

mild and severe intensity. How this happens has not

been explained (Djuardi, 2021). The high prevalence

of A. lumbricoides and T. trichiura infections in this

study indicates that oral-fecal transmission is more

common than transmission through skin penetration

(in hookworm infections) especially in children.

Other factors examined in this study were difficult

access to health centers and/or midwives (81.9%),

lack of access to water sources (13.8%) and poor

sanitation (87.3%) which of course could contribute

to the high incidence of intestinal parasitic infections

and nutritional problems among children in the area

(Djuardi, 2021).

Research conducted by Grimers showed that the

prevalence of hookworm infection was 18%, Ascaris

lumbricoides 4.8%, Trichuris trichiura 0.6% and S.

mansoni 0.3%. The high number of hookworm

infections in this study is known to be related to

inadequate sanitation, namely the absence of latrines

and open defecation. Apart from that, data was also

obtained on the prevalence of anemia of 23%,

stunting of 28% and wasting of 14%. Statistically,

there is no significant relationship between sanitation

and hookworms or between hookworms and anemia,

stunting or wasting (Grimes, 2017).

In Hailegebriel's study, 52.4% of subjects were

positive for one or more intestinal parasites. The

prevalence of multiple intestinal parasitic infections

is quite large, namely 6.3%. The most frequently

detected intestinal parasitic infections were E.

histolytica/dispar (16.8%), hookworm (14.7%) and

A. lumbricoides (13.6%). Based on the multivariate

analysis that was carried out, the predictors of

intestinal parasitic infection in this study were

unclean nails, irregular hand washing habits and

maternal education.

Nutritional problems occurred in 41.6% of

subjects, consisting of 18.3% stunting, 26.7% wasting

and 25.9% were underweight. Almost half of the

study subjects experienced 2 or more nutritional

problems at one time. Of the 18.3% of subjects who

experienced stunting, 20% of them experienced

severe stunting (HAZ<-3SD). Based on further

analysis, it is known that subjects born to families

with a monthly income of less than 1500 birr (around

Rp. 479,000.00), the frequency of eating a maximum

of 3 times in 1 day and the presence of intestinal

parasitic infections are the main predisposing factors

for malnutrition in children (Hailegebriel, 2018).

Mekonnen's research showed that research

subjects were infected with 8 species of intestinal

parasites, namely Trichuris trichiura, Ascaris

lumbricoides, hookworm, H.nana, E.histolytica,

E.vermicularis, G.lamblia, and S.mansoni . The

highest prevalence of intestinal parasitic infections is

infection due to mild intensity STH, namely 55% with

the most infections caused by T. trichiura (34.9%).

Ascaris lumbricoides and hookworm were detected in

28.5% and 11.4%. The highest STH infection

occurred in children with dirty nails (63.5%).

Children who have the habit of defecating in the open

(52.7%) have a 1.9 times higher risk of developing

STH infection. Likewise, children who are

accustomed to not wearing footwear have a 2.2 times

higher risk of being infected with hookworms than

children who wear shoes. The prevalence of stunting

is 21%. The results of multivariate analysis show that

T. trichiura infection is the main predictor of stunting

in children (Mekonnen, 2020).

Muslimah research in 2020 gave results of a

stunting prevalence of 46.5% and intestinal worm

infections of 41% in children aged 6 to 12 years.

There is an effect of worm infections on the incidence

of stunting where children with worm infections have

a 2.11 times greater probability of experiencing

stunting than children without intestinal worm

infections (Muslimah, 2020).

Yoseph's research stated that the total prevalence

of intestinal parasitic infections was 48.7%,

consisting of Giardia lamblia infections (10.45%),

Entamoeba hystolitica (4.66%), Ascaris lumbricoides

(10.77%), hookworms (7.88%). %), Trichiura

trichiura (6.1%), Strongyloides stercoralis (1.6%)

and Taenia sp (1.3%). About a quarter (22%) of

children were moderately infected and 5.94% had

multiple intestinal parasitic infections. The

prevalence of stunting is 39.3% and 3.4% of them

experience severe stunting. Other nutritional

problems are underweight 24% and wasting 11.6%.

The prevalence of stunting in children infected with

intestinal parasites (59.4%) was significantly higher

than the prevalence in uninfected children (20.6%).

Almost all (92.53%) children infected with Ascaris

lumbricoides experienced stunting. Likewise, in other

intestinal parasitic infections, such as in people with

hookworm infections, the prevalence of stunting is

89.79%, in G. lamblia infections it is 86.20%, E.

histolytica is 72.24%, T. trichiura is 71%, Taenia sp.

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191

By 50% and Strongyloides stercoralis by 50%.

Statistically, there is a significant relationship

between stunting and infection with hookworms,

G.lamblia , E.histolytica and T.trichiura . Children

infected with intestinal parasites have a 5.45 times

greater risk of experiencing stunting compared to

those who are not infected (Yoeph, 2020).

Based on the results of these six studies, it is clear

that the prevalence of intestinal parasitic infections is

still high. Intestinal parasitic infections occur in

various ages of children, even in babies as young as 6

months (Yoseph, 2020). The availability of adequate

sanitation facilities is very important because

otherwise it will be possible for contamination of

water and food with human waste, especially if the

habit of defecating in open fields continues. The habit

of not using footwear can occur because there is still

a lack of public knowledge and awareness about how

this intestinal parasite can infect humans.

Intestinal parasitic infections can cause various

impacts on the host. Intestinal worms can reduce a

child's appetite and cause competition between hosts

and parasites. Lack of carbohydrates, protein,

nutrients, and blood can reduce the adequacy needed

by the body, thereby reducing the quality of human

resources (Muslimah, 2020; Jourdan, 2018).

Intestinal protozoal infections often cause complaints

of diarrhea. Research shows that 25% of stunting

cases are associated with five or more episodes of

diarrhea (Millward, 2017). Exposure to these

pathogens can cause disruption of intestinal structure

and function called environmental enteric

dysfunction (EED). This condition is a reversible

condition, characterized by villous atrophy of

intestinal mucosal cells, crypt hyperplasia, increased

permeability, and inflammatory cell infiltration. This

can result in disruption of the intestinal immune

response, reducing the delivery, absorption and

utilization of nutrients resulting in a state of

nutritional deficiency. A state of nutritional

deficiency can then result in damage to epithelial

tissue renewal, maturation and proliferation of

intestinal cells and pancreatic b cells, thus disrupting

linear growth (Budge, 2019).

Increased intestinal permeability can be

determined from the lactose/mannitol ratio (Budge,

2019). Research shows that this ratio tends to be

higher in children with infections, especially

Cryptosporidium infections sp. and Giardia sp

(Budge, 2019). Choudhry's research has shown that

C. parvum infection can alter intestinal barrier

function by reducing the integrity of the intestinal

epithelium through reduced TER (Transepithelial

Electrical Resistance) associated with

downregulation of the claudin-4 protein (Choudry,

2021). In giardiasis there is malabsorption of fat,

xylose and vitamin B12. Mannose-binding lectin

mediates parasite adhesion to brush border

enterocytes. Increased apoptosis, loosening of

enterocyte adhesions at tight junctions, and damage

to the enterocyte membrane lumen contribute to

impaired digestion and nutrient absorption (Wright,

2012).

The six studies above also provide results that the

prevalence of nutritional problems in children is still

high, namely in the range of 18.3% to 46.5%.

Nutritional problems detected in the research subjects

included underweight, thinness, stunting, wasting and

anemia. Underweight, can also be called

underweight, is the child's nutritional status based on

body weight for age with a Z score of -3SD to -2SD.

Stunting is short stature, a child's nutritional status

based on length or height per age with a Z score of -

3SD to -2 SD. Wasting, which can also be called

undernutrition, is a child's nutritional status based on

weight per body length, weight per child's height, or

body mass index (BMI) per child aged 0 to 60 months

with a Z score of -3SD to -2SD . Thinnes, also called

malnutrition, is a category of children's nutritional

status based on BMI per child aged 5 to 18 years with

a Z score of -3SD to -2SD (Minister of Health of the

Republic of Indonesia, 2020).

Monitoring intestinal parasitic infections and

children's nutritional status is very important to pay

attention to because it greatly affects their health

condition and academic achievement (Hailegebriel,

2018). Apart from carrying out nutritional

interventions, it is also necessary to consider the

importance of carrying out environmental

interventions including water, sanitation and hygiene

to prevent the occurrence of infectious diseases,

including intestinal parasitic infections (Grimes,

2017).

5.1 Research Limitations

In this research there are still several limitations,

including that this research only accesses free

published journals. Sources for unpublished articles

are still limited because they are limited to digital

searches due to the COVID 19 pandemic which still

limits activities. Apart from that, this research is

limited to analyzing the relationship between only

two variables, namely intestinal parasitic infections

and the incidence of stunting in children. There are

still other variables such as intensity of parasite

infection, Hb levels, body weight and body mass

index that can be analyzed in further research.

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6 CONCLUSSION

Research that meets the criteria to be tested in meta-

analysis is six articles (journals) with heterogeneous

variations. The effect size used is the odds ratio

where the combined effect results show a p value

<0.05, which means there is an influence between

intestinal parasitic infections, namely intestinal worm

infections and intestinal protozoa on the incidence of

stunting in children. Further research is needed

regarding other nutritional status variables such as

underweight, thinness, and wasting. Apart from that,

it is also necessary to add reading sources, both text

books and related journals, to add references for

further research.

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