Al-Sihah : Public Health Science Journal 44-52

Environmental Sanitation as Risk Factors for Intestinal Protozoa

Infection among Stunted Children in Sugerkidul Village, Indonesia

Hanu N. Septian1 , Erma Sulistyaningsih*2 , Angga M. Raharjo3 , Bagus Hermansyah4

Wiwien S. Utami5 , Yunita Armiyanti6

1, 2, 4, 5, 6
Department of Parasitology, University of Jember, Jember, Indonesia
3
Department of Public Health, University of Jember, Jember, Indonesia

DOI: 10.24252/al-sihah.v15i1.35378
Received: 18 March 2023 / In Reviewed: 9 May 2023 / Accepted: 13 June 2023 / Available online: 29 June 2023
©The Authors 2023. This is an open access article under the CC BY-NC-SA 4.0 license

ABSTRACT
Stunting, a prevalent health issue in Indonesia, has been found to have a significant impact on the overall well-being of chil-
dren, with a prevalence rate of 24.4%. This condition not only affects physical growth but also puts children at a heightened
risk of various infections, including those caused by intestinal protozoa. Therefore, this study aimed to determine the relation-
ship between personal hygiene parenting style and environmental sanitation with intestinal protozoa infection among stunted
children in Sugerkidul Village, Jember District, Indonesia. The participants included were 30 stunted children. Questionnaires
were used to collect data on personal hygiene parenting style and environmental sanitation, while microscopic stool examina-
tion was conducted to identify intestinal protozoa infection. The results showed that 26.7% of stunted children were infected
with intestinal protozoa such as Giardia lamblia (13.3%), Blastocystis hominins (3.3%), and Cryptosporidium parvum (10%).
Statistical analysis using Fisher's exact test showed a significant association between environmental sanitation and intestinal
protozoa infection. However, there was no association between personal hygiene parenting style and this infection among
stunted children in Sugerkidul Village. Therefore, to prevent intestinal protozoa infection, it is necessary to improve environ-
mental sanitation.

ABSTRAK
Stunting merupakan masalah kesehatan yang penting di Indonesia, dengan prevalensi sebesar 24.4%. Gangguan ini
mempengaruhi keseluruhan pertumbuhan dan perkembangan balita serta mengakibatkan risiko infeksi yang lebih tinggi,
termasuk infeksi protozoa usus. Penelitian ini bertujuan untuk menganalisis hubungan antara pola asuh kebersihan diri dan
sanitasi lingkungan dengan kejadian infeksi protozoa usus pada balita stunting di Desa Sugerkidul, Jember, Indonesia.
Sebanyak 30 balita stunting dilibatkan dalam penelitian ini. Data pola asuh kebersihan diri dan sanitasi lingkungan dik-
umpulkan menggunakan kuesioner dan infeksi protozoa usus diidentifikasi dengan pemeriksaan mikroskopis feses. Infeksi
protozoa usus ditemukan pada 26.7% balita stunting dan protozoa usus yang teridentifikasi antara lain Giardia lamblia
(3.3%), Blastocystis hominis (3.3%), dan Cryptosporidium parvum (10%). Analisis statistik menggunakan Fischer exact test
menunjukkan hubungan yang signifikan antara sanitasi lingkungan dengan kejadian infeksi protozoa usus, tetapi tidak signif-
ikan pada hubungan antara pola asuh kebersihan diri dengan kejadian infeksi protozoa usus pada balita stunting di Desa
Sugerkidul, Jember. Oleh karena itu, peningkatan sanitasi lingkungan sangat penting dalam upaya mencegah infeksi proto-
zoa usus terutama pada balita stunting di wilayah ini.

GRAPHICAL ABSTRACT
Keyword
child
hygiene
intestinal diseases
protozoan infections
sanitation

* Correspondence
Jl. Mastrip No.69, Kec. Sumbersari, Kabupaten Jember,
PO.Box 68124 Jawa Timur, Indonesia
Email: sulistyaningsih.fk@unej.ac.id

Volume 15, Nomor 1, January-June 2023 ISSN-P : 2086-2040

ISSN-E : 2548-5334
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INTRODUCTION Intestinal protozoa infection poses a

Stunting, characterized by impaired risk to individuals, with children being particu-
growth and development in children, is a signif- larly susceptible (Hajissa et al., 2022). This in-
icant health problem observed in many develop- creased vulnerability among children can be
ing countries, including Indonesia, where it is attributed to their dynamic behavior, limited
particularly prevalent. According to the Indone- knowledge of hygiene practices, and the pres-
sia Nutritional Status Survey of the Ministry of ence of intestinal protozoa contamination
Health, the incidence rate of this disorder in the (Bahmani et al., 2017). The diseases usually
country was 24.4% in 2021. Other developing occur due to unhygienic toilet practices and in-
countries, such as Pakistan, India, and Ethiopia adequate hand hygiene during eating times
reported rates of 31.7%, 35.5%, and 37%, re- (Hajissa et al., 2022). Notably, children with
spectively (Mengesha et al., 2021; Siddiqa et poor hygiene practices have a higher likelihood
al., 2022; Varghese et al., 2022). East Java of infection (Galgamuwa et al., 2016). s guardi-
province was ranked 25th rank in terms of stunt- ans, parents play a crucial role in ensuring their
ing prevalence in Indonesia in 2021, with a rate children's hygiene, thereby preventing such in-
of 23.5%, and the district with the highest con- fections (Pérez Pico et al., 2022). The increase
tribution was Jember, including SugerKidul vil- in risk of infection is attributed to poor hygiene
lage (Kementerian Kesehatan RI, 2021). Stunt- practices of mothers (Wolde et al., 2022). Fur-
ing is a complex health issue influenced by mul- thermore, environmental sanitation is associated
tiple factors, and infection is recognized as an with intestinal protozoa infection (Bahmani et
important risk factor in its development (Akrom al., 2017). Poor environmental sanitation due to
et al., 2022). Among various types of infections, feces contamination can increase risk of this
gastrointestinal infection, including intestinal disease (Wahdini et al., 2021). Additionally,
protozoa, are commonly reported (Fauziah et protozoa can contaminate and spread through
al., 2022). It is believed that these infections water, thereby causing infection (Hoseinzadeh
may contribute to stunting by causing nutrient et al., 2021).
malabsorption and direct nutrient loss in affect- Previous studies have demonstrated the
ed individuals (Rajoo et al., 2017). determinants of personal hygiene, such as nail
The prevalence of intestinal protozoa and hand hygiene (Mohammed et al., 2022).
infection remains high in Indonesia. A previous Environmental factors such as clean water facil-
study reported that the incidence of this infec- ities, latrine conditions, and waste management
tion was rated at 20% (Wahdini et al., 2021), were associated with intestinal protozoa infec-
and is generally higher in children under 10 tion (Muhajir et al., 2019). Furthermore, studies
years old (Dobo, 2018). Children under 5 years showed the correlation between environmental
had a rate of 36.8%, higher than those between sanitation and personal hygiene with intestinal
5 and 8 years, which was only 5.7% (Ntulume protozoa infection in children (Balbino et al.,
et al., 2017). The common protozoa that infect 2023; Njambi et al., 2020; Tambunan &
children under 5 years are Entamoeba histolyti- Panggabean, 2021). However, study on the par-
ca, Giardia lamblia, Cryptosporidium parvum, enting style aspect and environmental sanitation
and Blastocystis hominis (Boughattas et al., in stunted children remains limited. Therefore,
2017; Tegen et al., 2020; Wale & Gedefaw, this study analyzed personal hygiene's parenting
2022). style and environmental sanitation and their as-
sociation with intestinal protozoa infection.
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METHODS conducted using Fisher's exact test. Information

This was an observational study with a on personal hygiene parenting style and envi-
cross-sectional design, conducted from August ronmental sanitation were recategorized into
to December 2022. The participants were stunt- good and poor categories, which consisted of
ed children aged 12-59 months in Sugerkidul moderate and poor. The study was approved by
Village, Jember Regency, East Java Province, the Ethical Committee of the Faculty of Medi-
Indonesia. Informed consent was obtained from cine, University of Jember, with reference
the mother of the children. The process in- number 1668/H25.1.11/KE/2022.
volved a detailed explanation of the study's
procedures and subsequently signing the ap- RESULTS
proval. Finally, the participants in this study The characteristics of respondents in-
were 30 stunted children recruited by total sam- cluded gender and age of stunted children, edu-
pling technique. cation level, occupation of their mother, and
Data on personal hygiene parenting family income. The majority were girls
style including the cleanliness of nails and (56.7%) and aged between 24-35 months
hands, as well as environmental sanitation, (46.7%). Most of their mothers were young,
such as water facilities, toilet conditions, waste aged 20 to 25 (63.3%), have a low education
disposal, and garbage condition, were obtained level (76.7%), and are housewives (73.3%).
by a questionnaire that was adapted from a pre- Additionally, 83.3% have a low family income,
vious study and consulted with experts as shown in table 1. The respondents at the pro-
(Kementerian Kesehatan RI, 2021; Tambunan portion of 36.7% and 46.7% had a moderate
& Panggabean, 2021). The validity and relia- personal hygiene parenting style and good as
bility of the questionnaire were determined us- well as moderate environmental sanitation, re-
ing Pearson bivariate test and Cronbach's alpha spectively, as presented in table 1.
value, respectively. Personal hygiene parenting Microscopic stool examination showed
style and environmental sanitation were scored that 8 respondents (26.7%) were positive for
and classified into 3 categories, namely good, intestinal protozoa. The identified protozoa
moderate, and poor. Microscopic stool exami- were Giardia lamblia, Cryptosporidium par-
nation was conducted at the Laboratory of Par- vum, and Blastocystis hominis, with G. lamblia
asitology, Faculty of Medicine, University of having the highest percentage of 13.3%. How-
Jember. The stools were examined using the ever, no Entamoeba histolytica was detected,
direct smear method to detect protozoa, includ- as indicated in table 1.
ing Entamoeba histolytica, Giardia lamblia, The statistical analysis presented sig-
and Blastocystis hominis, while Ziehl Neelsen nificant value and odds ratio. Personal hygiene
staining technique to detect Cryptosporidium parenting style has a significance value of
parvum. The tools and materials utilized were 0.154, indicating that it is not significantly as-
centrifuge tube, vortex, glass slide, microscope, sociated with intestinal protozoa infection.
aqua dest solution, 1% Lugol solution, metha- However, for environmental sanitation it was a
nol, ZN A solution (Carbol fushin), ZN B solu- 0.03 significance value, meaning there is a sig-
tion (HCL and ethanol), and ZN C solution nificant association. The odd ratio for personal
(Malachite green 0.4%). hygiene parenting style and environmental san-
Data were presented in frequency and itation were 4.846 and 10.111, respectively, as
percentage and the intervariable analysis was shown in table 2.
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Table 1
Distribution of Characteristic of Respondents, Personal Hygiene and Environmental Sanitation
Characteristic of Respondent Frequency Percentage
Stunted Children Gender
Male 17 56.67
Female 13 43.33
Stunted Children Age (month)
12-33 6 20.00
24-35 14 46.67
36-47 7 23.33
48-59 3 10.00
Mother's Age (years)
20-25 19 63.33
26-35 10 33.33
36-40 1 3.33
Mother's Education
Low 23 76.67
High 7 23.33
Mother's Work Status
Housewife 22 73.33
Working Mother 8 26.67
Family Income
Low 25 83.33
Moderate 5 16.67
Personal Hygiene
Good 10 33.33
Moderate 11 36.67
Poor 9 30.00
Environmental Sanitation
Good 14 46.67
Moderate 14 46.67
Poor 2 6.67
Intestinal Protozoa Infection
Positive 8 26.67
Negative 22 73.33
Protozoa Species*
Entamoeba Histolytica 0 0.00
Giardia Lamblia 4 13.33
Cryptosporidium Parvum 3 10.00
Blastocytis Hominis 1 3.33
Note: *= There are 8 from 30 children diagnosed with intestinal protozoa infection.

DISCUSSION early marriages in Sugerkidul Village. Young

Stunted children in this study were pre- mothers usually need to gain better knowledge
dominantly female and primarily between the and skills in caring for children. This is in ac-
age of 24 and 35 months of age when cognitive cordance with their low education levels which
and motoric development occurs rapidly. This makes it difficult to receive information on nu-
period needs high-quality and quantity nutrition, trition and child care, thereby increasing risk of
otherwise, they will be at an increased risk of raising stunted children. Despite most mothers
stunting, and this is in line with previous studies being housewives who have more caring time, a
(Manggala et al., 2018; Rajoo et al., 2017). An- low family income affects the ability to provide
other interesting result is that mothers of chil- good food and nutrition, as reported by a previ-
dren are between the age of 20 and 25 years, ous study (Titaley et al., 2019).
and this can be because of the high number of Data on personal hygiene parenting
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Table 2
Risk Factors for Intestinal Protozoa Infection

Intestinal Protozoa Infection

Variables Positive Negative Significance Odds Ratio
Frequency Percentage Frequency Percentage
Personal Hygiene
Good 1 12.5 9 40.9 0.150 4.85
Poor 7 87.5 13 59.1
Environmental Sanitation
Good 1 12.5 13 59.1 0.030* 10.11
Poor 7 87.5 9 40.9
Note: *= Environmental sanitation has a significant relationship using the fisher's exact test (sig <0,05).

style showed variable results but slightly differ- often occurs in children (Waldram et al., 2017).
ent between categories. Mothers ignore the According to the previous study, it is the most
children's hands and nail cleanliness habits, common infection in children under the age of
such as failing to ensure hand washing before 5 (Deka et al., 2022). G. lamblia infection usu-
eating, after defecating, and after playing. ally occurs due to environmental sanitation
Some do not regularly cut their children's nails conditions (Hajare et al., 2022). Other infection
routinely every week, hence, they become dirty identified in this study were Cryptosporidium
and unhygienic. This could be due to low edu- parvum and B. hominis. Previous studies stated
cation levels, which causes poor parenting that they can be identified among children un-
styles (Muryanti et al., 2016). The majority of der the age of 5 (Tamomh et al., 2021; Salehi
environmental sanitation in this study was good Kahish et al., 2021). These opportunistic proto-
and moderate, and this is in line with the Jem- zoa often attack humans with low immunity
ber health statistic in 2021. However, some (Bednarska et al., 2018). However, no cases of
participants have poor environmental sanita- E. histolytica were detected in the study.
tion, especially in the areas of waste disposal According to a previous study, person-
and garbage facilities. al hygiene parenting style has no significant
Approximately 26.7% of respondents association with intestinal protozoa infection
have intestinal protozoa infection. Children (Tsegaye et al., 2020). However, it was mostly
under the age of 5 have a higher risk of this identified among positively infected stunted
disease, due to uncontrolled behavior children (Gizaw et al., 2018). Another study
(Tambunan & Panggabean, 2021; Zemene & showed a significant association between per-
Shiferaw, 2018). This study was conducted sonal hygiene and intestinal protozoa infection
among stunted children, who are thought to be (Tambunan & Panggabean, 2021). Poor hy-
more susceptible to intestinal protozoa infec- giene parenting has risk of contracting this dis-
tion due to a lack of immune system, as report- ease. Furthermore, dirty nails and poor hand
ed in the previous study (Yoseph & Beyene, hygiene can raise risk of transmission (Berhe et
2020). Furthermore, they have a high rate of al., 2020). Some indicators of personal hygiene
infection due to a lack of immune systems parenting style, include hand and food hygiene
(Akrom et al., 2022). which is essential among the caregivers of chil-
The most common type of intestinal dren under the age of 2 who cannot eat person-
protozoa in this study is G. lamblia which is ally. A previous study showed that most moth-
high at 43% in low-income countries, and most ers had poor hand hygiene behavior (El-Aal et
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al., 2022). According to another study, the pres- lighted the importance of environmental sanita-
ence of dirty hands in mothers can lead to diar- tion on protozoa infection. Increasing public
rhea in children, which could be caused by pro- awareness regarding proper maintenance and
tozoa infection (Taddese et al., 2020). Food hy- improvement of environmental sanitation is piv-
giene also plays a role in the existence of this otal in preventing health problems, including
disease, as unhygienic food serves as a suitable stunting as a growth disorder and microorgan-
medium for protozoa cyst (Luz et al., 2017). ism infection such as intestinal protozoa.
The odds ratio value of 4.84 indicated that poor
hygiene parenting can increase risk of infection CONCLUSIONS
by 4.85 times. Therefore, mothers should give This study found a high prevalence of
more attention to children's hygiene to prevent protozoa infection, including G. lamblia, B.
intestinal protozoa infection. hominis, and C. parvum, among stunted chil-
In this study, environmental sanitation dren in Sugerkidul Village, Jember. Further-
showed a significant association with intestinal more, environmental sanitation was observed to
protozoa infection (Yoseph & Beyene, 2020). play a significant role in the occurrence of intes-
The odd ratio also had a similar indication. The tinal protozoa infection, while personal hygiene
active behavior of children at home as well as parenting style does not exhibit a direct associa-
around their environment has a higher potential tion. However, it is important to note that poor
for exposure to microorganisms, including pro- personal hygiene parenting style carries a 4.84
tozoa. Notably, children who engage in play times higher risk of this disease. Therefore, it is
activities within unclean areas show a signifi- crucial for mothers or caregivers to enhance
cant association with an increased risk of para- their awareness and adopt good personal hy-
site infection (Eyasu et al., 2022). Some factors giene parenting practices, along with maintain-
correlate with environmental sanitation and pro- ing proper environmental sanitation.
tozoa infection, such as protozoa contamination Despite the inclusion of all stunted chil-
in water, food, or other objects. The quality of dren in Sugerkidul Village, Jember, it is im-
water plays a significant role in the relationship portant to acknowledge the limited sample size
with this infection (Wale & Gedefaw, 2022). of this study. Furthermore, the study does not
Furthermore, the distance between clean water explore other potential risk factors for intestinal
and pollutant sources could be factors. This is protozoa infection in children, such as food hy-
because a minimum distance of 10 m is needed giene. Therefore, future research involving larg-
to decrease risk of contamination (Muhajir et er populations and considering various risk fac-
al., 2019). Latrine conditions, wastewater dis- tors could provide valuable insights. The results
posal facilities, and the availability of trash cans of this study can serve as a reference for the
are associated with the occurrence of this dis- government and other stakeholders in devising
ease (Deka et al., 2022; Fuhrimann et al., 2016). approaches to prevent intestinal protozoa infec-
The study has shown that environmen- tion and further reduce the prevalence of stunt-
tal sanitation is a vital factors in stunting ing. The significant association between envi-
(Gizaw et al., 2022), and it has a significant as- ronmental sanitation and intestinal protozoa
sociation with protozoa infection among stunted infection in stunted children underscores its cru-
children. However, the study design which in- cial role in designing comprehensive strategies
cluded only stunted children as participants, to address health problems associated with
lead to a limited sample size. This result high- stunting.
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ACKNOWLEDGEMENT Bednarska, M., Jankowska, I., Pawelas, A., Piwczyńska, K.,

The author would like thank to University of Jember for provid- Bajer, A., Wolska-Kuśnierz, B., Wielopolska, M., &
Welc-Falęciak, R. (2018). Prevalence of Cryptosporidi-
ing funding and support for this research. Our acknowledgment
um, Blastocystis, and other opportunistic infections in
also conveyed to respondents who have agreed to be involved in patients with primary and acquired immunodeficiency.
the study. Parasitology Research, 117(9), 2869–2879.
https://doi.org/10.1007/s00436-018-5976-6
FUNDING Berhe, B., Mardu, F., Tesfay, K., Legese, H., Adhanom, G.,
This research was funded by University of Jember through the Haileslasie, H., Gebremichail, G., Tesfanchal, B.,
Grant of Research and Community Service Group No. Shishay, N., & Negash, H. (2020). More than half preva-
lence of protozoan parasitic infections among diarrheic
4484/UN25.3.1/LT/2022. outpatients in eastern tigrai, ethiopia, 2019; a cross-
sectional study. Infection and Drug Resistance, 13, 27–
AUTHORS’ CONTRIBUTIONS 34. https://doi.org/10.2147/IDR.S238493
Hanu N. Septian wrote the manuscript, collected data, analyzed Boughattas, S., Behnke, J. M., Al-Ansari, K., Sharma, A., Abu-
the data, performed the field work. Erma Sulistyaningsih, wrote Alainin, W., Al-Thani, A., & Abu-Madi, M. A. (2017).
the manuscript, acquired and analyzed the data, reviewed and Molecular analysis of the enteric protozoa associated with
acute diarrhea in hospitalized children. Frontiers in Cel-
revised the manuscript. Angga M. Raharjo reviewed the manu-
lular and Infection Microbiology, 7(343), 1–10.
script. Bagus Hermansyah, Wiwien S. Utami, and Yunita Armi- https://doi.org/10.3389/fcimb.2017.00343
yanti revised the manuscript. All authors designed the study,
Deka, S., Kalita, D., & Hazarika, N. K. (2022). Prevalence and
formulated the concept and approved the final manuscript. Risk Factors of Intestinal Parasitic Infection in Un-
der‑Five Children With Malnutrition: A Hospital Based
AUTHORS’ INFORMATION Cross‑Sectional Study. Journal of Family Medicine and
Dr. rer. bio. hum. dr. Erma Sulistyaningsih, M.Sc., Primary Care, 11(6), 2794–2801.
https://doi.org/10.4103/jfmpc.jfmpc_1742_21
GCert.AgHealthMed is an associate professor in Department of
Parasitology Faculty of Medicine University of Jember, Jember, Dobo, B. (2018). Prevalence of intestinal protozoan infection
Indonesia. Angga Mardro Raharjo, MD, Pulmonologist Sp.P is among patients in Hawassa city administration millenni-
um health center, Ethiopia. Journal of Applied Biotech-
an assistant professor in Department of Public Health Faculty of nology & Bioengineering, 5(4), 206–210.
Medicine University of Jember, Jember, Indonesia. Bagus Her- https://doi.org/10.15406/jabb.2018.05.00139
mansyah, MD., M.Biomed. is an assistant professor in Depart-
El-Aal, B. G. A., Nady, S. E., Shokr, E. A., & Shokry, M. W.
ment of Parasitology Faculty of Medicine University of Jember, (2022). Awareness And Practices Of Preventive Behav-
Jember, Indonesia. Dr. Wiwien Sugih Utami, MD., M.Sc. is an iors Toward Intestinal Parasitic Infection Among Mothers
assistant professor in Department of Parasitology Faculty of Of Preschool Children. Journal of Positive School Psy-
chology, 6(8), 6290–6305.
Medicine University of Jember, Jember, Indonesia. Dr. Yunita
https://journalppw.com/index.php/jpsp/article/view/10926
Armiyanti, MD., M.Kes., Sp.Park. is an assistant professor in
Department of Parasitology Faculty of Medicine University of Eyasu, A., Molla, M., Kefale, B., Sisay, W., Andargie, Y.,
Kebede, F., & Jemere, T. (2022). Prevalence and Associ-
Jember, Jember, Indonesia ated Risk Factors of Endoparasites among Under-Five
Children in Debre Tabor Comprehensive Specialized
COMPETING INTERESTS Hospital, Debre Tabor, Northwest Ethiopia: A Cross-
The authors confirm that all of the text, figures, and tables in the Sectional Study. Journal of Parasitology Research, 2022,
1–10. https://doi.org/10.1155/2022/6917355
submitted manuscript work are original work created by the
authors and that there are no competing professional, financial, or Fauziah, N., Aviani, J. K., Agrianfanny, Y. N., & Fatimah, S. N.
(2022). Intestinal Parasitic Infection and Nutritional Sta-
personal interests from other parties.
tus in Children under Five Years Old: A Systematic Re-
view. Tropical Medicine and Infectious Disease, 7(11),
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