Mono-Parasitic and Poly-Parasitic Intestinal Infections among Children Aged 36–45 Months in East Nusa Tenggara, Indonesia
by
, , ,
Alpha F. Athiyyah
1,2,
Ingrid S. Surono
3,*,
Reza G. Ranuh
1,2,
Andy Darma
1,2,
Sukmawati Basuki
4,5,
Lynda Rossyanti
4,5,
Subijanto M. Sudarmo
1,2 and
Koen Venema
6 1
Department of Child Health, Faculty of Medicine, Universitas Airlangga, Surabaya 60286, Indonesia
2
Department of Child Health, Dr. Soetmo General Hospital, Surabaya 60286, Indonesia
3
Food Technology Department, Faculty of Engineering, Bina Nusantara University, Jakarta 11480, Indonesia
4
Department of Medical Parasitology, Faculty of Medicine, Universitas Airlangga, Surabaya 60115, Indonesia
5
Malaria Study Group/Laboratory of Malaria, Institute of Tropical Disease, Universitas Airlangga, Surabaya 60286, Indonesia
6
Centre for Health Eating & Food Innovation, Maastricht University–Campus Venlo, 5928 SZ Venlo, The Netherlands
*
Author to whom correspondence should be addressed.
Trop. Med. Infect. Dis. 2023, 8(1), 45; https://doi.org/10.3390/tropicalmed8010045
Submission received: 29 November 2022
/
Revised: 29 December 2022
/
Accepted: 4 January 2023
/
Published: 6 January 2023
(This article belongs to the Special Issue Host-Parasite-Environment Interactions)
Abstract
:The prevalence of intestinal parasitic infection remains high in developing countries, especially because of geographic and socio-demographic factors. This study aimed to evaluate intestinal parasitic infection, as well as its risk factors, among children aged 36–45 months in a rural area (North Kodi) and an urban area (Kupang) of East Nusa Tenggara, Indonesia. Anthropometry, socio-demographic factors and personal hygiene practices were assessed. A total of 214 children participated in the study, and 200 stool samples were collected for intestinal parasite examination. Approximately 30.5% (61/200) of the children were infected with one or more intestinal parasites (67.2%; 41/61 being mono-parasitic infections and 32.8%; 20/61 being poly-parasitic infections). A total of 85 intestinal parasites were detected, consisting of 35.3% (30/85) protozoa and 64.7% (55/85) helminths. The predominant protozoa were Giardia lamblia (43%; 13/30) and Blastocystis spp. (33.3%; 10/30), whereas the predominant helminths were Trichuris trichiura (50.9%; 28/55) and Ascaris lumbricoides (43.6%; 24/55). Moreover, intestinal parasitic infection was associated with rural area (OR 4.5; 95%CI 2.3–8.6); the absence of treatment with deworming drugs (OR 2.56; 95%CI 1.3–5.0); sanitation facilities without a septic tank (OR 4.3; 95%CI 2.1–8.5); unclean water as a source of drinking water (OR 4.67; 95%CI 2.4–9.4); no handwashing practice after defecation (OR 3.2; 95%CI 1.4–7.3); and stunted children (OR 4.4; 95%CI 2.3–8.3). In conclusion, poly-parasitic infections were common in this study. Poor personal hygiene practice and sanitation factors contributed to the high prevalence of intestinal parasitic infection in 36–45-month-old children in East Nusa Tenggara, Indonesia.
1. Introduction
Intestinal parasitic infections, particularly those of protozoa and helminth, are responsible for morbidity in children worldwide and represent a major public health problem in developing countries that is often neglected [1,2,3]. Children are particularly susceptible to infection by these microorganisms, which further negatively affects their nutritional status and physical development [1,2]. The global prevalence of intestinal parasitic infections remains high, with approximately 3.5 billion people infected and more than 200,000 deaths [4,5]. Based on data from 118 countries, the highest prevalence for soil-transmitted helminth infections (STHs) is detected in South Asia, Southeast Asia, and Sub-Saharan Africa. Of these infections, 67.3% occur in Asia [6]. In Indonesia, the prevalence of helminth infections is reported to vary between 2.5 and 62% [7]. East Nusa Tenggara, Indonesia, as a remote area, still experiences a high prevalence of parasitic infection. The STHs prevalence in Southwest Sumba and West Sumba in East Nusa Tenggara is >20%; however, the exact prevalence is difficult to ascertain. The prevalence of protozoan infections with Entamoeba histolytica, Giardia lamblia, and Blastocystis hominis (Bh) is reported to be 17.9% (76/424), 4.5% (19/424), and 34.4% (146/424), respectively [8].
In low- and middle-income countries, exposure to inadequate drinking water, sanitation, hygiene conditions, and hygiene behaviors are attributed to a greater proportion of intestinal parasite infections [9]. A recent systematic review reported that age, sex, residence, toilet facilities, washing hands with soap before a meal, shoe-wearing habits, trimming nails, eating undercooked food, personal hygiene and source of drinking water are the most risk factors for intestinal parasite infection [10]. Intestinal parasitic infections and their risk factors in Indonesia warrant further study. The current work was, therefore, carried out to evaluate the risk factors for intestinal parasitic infections among children aged 36–45 months in North Kodi and Kupang, East Nusa Tenggara, Indonesia.
2. Materials and Methods
2.1. Study Design and Ethical Clearance
A cross-sectional study was conducted on 214 children aged 36–45 months in Kupang and North Kodi, East Nusa Tenggara, Indonesia, from October to December 2021. The study protocol was approved by the Ethics Committee of the Research Institute of YARSI University, Jakarta, Indonesia, and registered at ClinicalTrials.gov with identifier number NCT05119218. The children’s parents or caregivers provided oral and written informed consent and signed a letter of consent before the children were included in the study.
2.2. Fecal Analysis and Parasitological Diagnosis
The parents/caregivers were instructed to collect each child’s stool and bring the stool specimen in a sterile container. All 200 collected stools were preserved in 10% formalin solution. The presence of parasites was detected via standard microscopy techniques (Olympus, Japan) using direct wet-mount smear methods, followed by staining with lugol solution, with six replications at the Laboratory of Malaria, Institute of Tropical Disease, Universitas Airlangga. The presence of eggs, larvae, trophozoites, or cysts was assessed for each type of helminth (Trichuris trichiura, Hookworm, Ascaris lumbricoides, and Hymenolepis diminuta) and protozoa (Entamoeba histolytica, Entamoeba coli, Giardia lamblia, and Blastocystis) spp., respectively. Positive parasitic infection was recorded by examining each prepared slide in which one or more parasites were detected. Mono-parasitic infection was defined as the presence of either one protozoan or one helminthic parasite in one child. Poly-parasitic infection was defined as (1) >1 positive protozoan parasites; (2) >1 helminthic parasites; and (3) mixed infection with both intestinal protozoan and helminthic parasites detected in one child.
2.3. Anthropometry
Height was measured using a wall stadiometer (Seca 208; precision, 0.1 cm) with the child’s head positioned according to the Frankfurt plane by trained nurses and general practitioners. Z-scores of height-for-age were calculated using the WHO AnthroPlus software provided by the World Health Organization, Geneva, Switzerland, in 2007 [11]. The height-for-age was classified as severely stunted (height for age < –3SD); stunted (–3SD to <–2SD); and normal (–2SD to +3SD). For analysis, the subjects were divided into the stunted group (if the subjects were severely stunted and stunted) and the normal group.
2.4. Subject Characteristics
A structured questionnaire was administered by two pediatricians, four general practitioners, nurses, laboratory technicians, and a community health care worker for face-to-face interviews with the respective child’s mother or caregiver, in order to collect sociodemographic information and hygiene practices. The independent variables were gender, locus of the rural (North Kodi) and urban (Kupang) area, mother’s education and occupation, family income, history of low birth weight, history of intake of deworming drugs in the last 6 months, family size, source of drinking water, type of sanitation facility, handwashing practice (before eating and after defecation), and handwashing facilities. Family size referred to the number of persons in the family and was categorized as small (<6 members), medium (6–8 members), and large (>8 members). Sanitation facility was defined as one that hygienically separates human feces from human contact and was categorized into a latrine with and without a septic tank. The mother’s education was divided into educated (elementary school, junior high school, senior high school, and university graduate) and uneducated. Family income was considered based on the regional minimum wage in each city and classified as lower than the regional minimum wage and equal to or greater than the regional minimum wage. The source of drinking water was divided into clean water (from mineral water, spring, tap water, and dug well) and unclear water (rainwater collection). Handwashing facilities were either fixed or mobile and included a sink with tap water and other models designated for handwashing.
2.5. Statistical Analyses
The data are presented as numbers and percentages for descriptive data. The chi-square and Fisher’s exact tests were used to assess differences in sociodemographic factors and hygiene practices between North Kodi and Kupang, as well as between stunted and normal children in categorical data. A univariate analysis was used to determine the odds ratio with the 95% confident interval of each variable that affected intestinal parasitic infection among children aged 36–45 months. Significance was set at p < 0.05. All statistical analyses were performed using the statistical program for social science (SPSS) Version 20.0 for Windows (SPSS Inc., Chicago, IL, USA).
3. Results
Intestinal Parasitic Infection and Risk Factors in 36–45-Month-Old Children in East Nusa Tenggara, Indonesia
This study included 214 children, and 200 stool samples were collected to analyze the parasitic infection status and its risk factors. The flow chart of this study is shown in Figure 1. Children with incomplete stool sample data were excluded from the study. Supplementary Data 1–3 show the demographic picture of Kupang and North Kodi. Kupang is a more densely populated urban area, whereas North Kodi is a rural area with mountains, hills and different types of housing compared with Kupang. A total of 30.5% (61/200) of the children were infected with intestinal parasites in this study, with 67.2% (41/61) of the cases being mono-parasitic infections and 32.8% (20/61) being poly-parasitic infections. Eighty-five intestinal parasites were detected in total, with 35.3% (30/85) being protozoan and 64.7% (55/85) being helminthic infections. Giardia lamblia (43%; 13/30) was the predominant protozoan parasite (Figure 2), whereas Trichuris trichiura (50.9%; 28/55) and Ascaris lumbricoides (43.6%; 24/55) were the predominant helminthic parasites (Figure 3) detected here.
Among children with mono-parasitic infection, 39% (16/41) had protozoan infection and 61% (25/41) had helminthic infection. Giardia lamblia and Blastocystis spp. were the most commonly detected parasites in protozoan mono-parasitic infection (50%; 8/16 and 25%; 4/16 of children, respectively). In turn, Trichuris trichiura and Ascaris lumbricoides were the most frequently detected parasites in children with helminthic mono-parasitic infection (44%; 11/25). In children with poly-parasitic infection, 10% (2/20) were infected with >1 protozoan, 50% (10/20) with >1 helminthic, and 40% (8/20) had mixed infections (both intestinal protozoan and helminthic parasites). Two children with >1 positive protozoa were detected to have Entamoeba coli–Blastocystis spp. and Entamoeba coli–Giardia lamblia. All children with >1 helminth infections were detected to have Ascaris lumbricoides–Trichuris trichiura. For mixed infection, two (25%) children were detected to have Ascaris lumbricoides–Trichuris trichiura–Blastocystis spp.; two (25%) with Trichuris trichiura–Giardia lamblia–Blastocystis spp.; two (25%) with Trichuris trichiura–Giardia lamblia; one (12.5%) with Trichuris trichiura–Blastocystis spp.; and one (12.5%) with Ascaris lumbricoides–Entamoeba coli. The microscopic findings of Giardia lamblia, Entamoeba coli, and Blasocystis spp. are depicted in Supplementary Data 4, 5, and 6.
More protozoa were detected in children from Kupang (60%; 18/30), whereas more helminths were detected in children from North Kodi (98.2%; 54/55) (Figure 2 and Figure 3). Entamoeba histolytica (100%; 1/1), Entamoeba coli (83.3%; 5/6), and Giardia lamblia (61.5%; 8/13) were more frequent in Kupang children, whereas helminthic infection was exclusively caused by Hymenolepis diminuta. Blastocystis spp. (60%; 6/10) was the predominant pathogen among the protozoan infections recorded in North Kodi. All Trichuris trichiura, Ascaris lumbricoides, and Hookworm infections were detected in North Kodi (Figure 2 and Figure 3). The majority of stunted children had intestinal protozoan (93.3%; 28/30) and helminthic (69.1%; 38/55) infection. Giardia lamblia was the predominant intestinal protozoa in stunted children (42.9%; 12/30), followed by Blastocystis spp. (33.3%; 10/30) (Figure 4). Trichuris trichiura was the predominant intestinal helminth (38.2%; 21/55), followed by Ascaris lumbricoides (25.5%; 14/55) (Figure 5).
The univariate analysis revealed that living in a rural area, lack of treatment with deworming drugs, a latrine without a septic tank, unclean water as the source of drinking water, no handwashing practice after defecation, and stunted children were risk factors for intestinal parasitic infection in this study (Table 1). Significant differences in the education level of the mother, family income, deworming status, source of drinking water, type of sanitation facility, handwashing practice (before eating as well as after defecation), and handwashing facility (p < 0.05) were observed between children from Kupang and those from North Kodi. Other characteristics are described in Table 2. A history of low birth weight, no deworming, drinking unclean water, using a latrine without a septic tank, and no handwashing practice (before eating and after defecation) were significantly different in stunted children compared with normal children (p < 0.05) (Table 3).
4. Discussion
The most common protozoa detected in all stool samples was Giardia lamblia, followed by Blastocystis spp. This result is in line with a study reported by Maru et al. in Ethiopia; among 235 infected children, the most prevalent parasite was Giardia lamblia (20%) [12]. Moreover, a study performed by Diarthini in Karangasem (Bali, Indonesia) reported that the prevalence of Blastocystis spp. in elementary school children was 33% (35/103), which was similar to the present study [13]. Both of those studies were conducted under geographic and socio-hygiene conditions that were similar to those of East Nusa Tenggara, which could explain the similar results. The most common helminth detected in this study was Ascaris lumbricoides, followed by Trichuris trichiura. Ascaris lumbricoides and Trichuris trichiura (whipworm) are soil-transmitted helminths (STHs) that are mostly found in tropical and subtropical areas [14,15,16]. A study performed by Pullan et al. in 118 countries revealed that both Ascaris lumbricoides and Trichuris trichiura were the predominant global STHs infection agents [6]. Wani et al. reported a similar prevalence in India. Among 2256 children, the prevalence of Ascaris lumbricoides was the highest (68.3%), followed by Trichuris trichiura (27.9%) [17]. Higher Trichuris trichiura and Ascaris lumbricoides rates were also found in a study reported by Sungkar et al. in Sumba, Indonesia. Among 88 children, the rate of Trichuris trichiura was 85.2%, whereas that of Ascaris lumbricoides was 71.6% [18].
In addition to mono-parasitic infection, we also found poly-parasitic infection in this study. Blastocystis spp. was the predominant protozoa involved in poly-parasitic infections. This result was in line with the study performed by Diarthini et al. in Karangasem, Bali, Indonesia. Blastocystis spp. is a predominant parasite in under-developed countries, especially in children. Blastocystis spp. is often found in poly-parasitic infections with Giardia lamblia, E. histolytica, and E. coli. Moreover, it is detected in mixed infection with Hookworm [13]. In turn, Ascaris lumbicoides and Trichuris trichiura are the predominant helminths involved in poly-parasitic infections. In endemic areas, especially in warm tropical and sub-tropical areas, poly-parasitic infections occur frequently and might result in the exacerbation of morbidity, as well as a greater intensity of infection. Both helminths are transmitted via the faecal–oral route, which, because the exposure is similar, leads to a positive association. Poly-parasitic infections have no specific gastrointestinal symptoms; therefore, affected children are often underdiagnosed. If left untreated, moderate-to-heavy poly-parasitic infection could lead to chronic effects on the growth of children [14,19].
The total prevalence of intestinal parasitic infections in rural areas is notably higher than that recorded in urban areas. North Kodi is a rural area located in Southwest Sumba, whereas Kupang is the capital city, i.e., an urban area, and the administrative center of East Nusa Tenggara [20,21]. The hygiene and sanitation practices and facilities in urban and rural areas are different. The source of drinking water, type of sanitation facility, handwashing practice, and handwashing facility in North Kodi were significantly inferior compared with Kupang. Poor personal hygiene, poor environmental sanitation, low social economy, and population density will lead to an increase in soil-transmitted helminth and protozoa infections through the soil [22,23]. A greater number of children and their parents had no handwashing facility and used a latrine without a septic tank in North Kodi. In another study reported by Mane et al., students in a rural area reported a higher percentage (37.7%) of non-availability of a place for handwashing inside the home compared with only 17.9% in an urban area [24]. Based on the research of Idowu et al., a greater number of respondents (parents) from a rural community used an open pit. This was followed by the practice of open defecation by 46.7% of the responders. In contrast, the majority of the parents or caregivers from an urban area (49.1%) reported that they throw their children’s feces into a water closet after they use a potty [25].
Darlan et al. reported a strong relationship between personal hygiene practices and environmental sanitation and the incidence of soil-transmitted helminthic infection [26]. Another study from Apidechkul (North Thailand) performed among hill-tribe school children showed that drinking water contaminated by soil was an important risk factor for intestinal parasitic infection [27]. The practice of poor hygiene behaviors leads to a higher prevalence of soil contamination. The soil around rural areas is profoundly contaminated with parasite eggs stemming from the tendency to defecate without using a septic tank; soil-transmitted helminths require soil for immature stage development, in order to be transmitted to a host [28,29,30]. Unclean water as the source of drinking water remains a potential risk for helminthic infections not only because of direct ingestion, but also due to the consumption of unwashed fruits and vegetables or those that are improperly cooked [31].
Our study found that the deworming programs in the rural area were less frequent (55%) compared with the urban area. This was in line with a study reported by Sungkar et al. The rate of STH in 88 children in Sumba significantly decreased after deworming using Albendazole (from 95.4% to 53.4%) [18]. Deworming programs are routinely provided by the Indonesian Ministry of Health, with the distribution of Albendazole through primary healthcare or school-based deworming programs. Several lines of evidence suggest that these deworming drugs are used for public health intervention for preventing soil-transmitted helminth infection, with a lesser impact on protozoa. However, the outcome of this prevention strategy also depends on the environmental conditions and requires regular monitoring to observe the soil-transmitted helminths and the possibility of re-infection, which warrants the administration of an additional or adjusted dose of deworming drugs [32,33].
The lack of periodic evaluation of the nutritional status was one of the limitations of this study. Moreover, because some data were incomplete, the analyses were not performed using the same sample size. Finally, a PCR examination was not included as a diagnostic method for parasites; rather, wet staining and microscopic observation alone were used here. Conversely, the strength of this study was the employment of many types of variables, which allowed us to more precisely assess the risk of parasitic infection. The sample size was sufficient, and we compared samples from different geographic and social-hygiene conditions.
5. Conclusions
Mono-intestinal parasitic infections were most common in children aged 36-45 months in East Nusa Tenggara, Indonesia. Total intestinal protozoan infection was detected more in the urban area, Kupang, with Giardia lamblia and Blastocystis spp. being the predominantly detected pathogens. The total helminthic infection prevalence was higher in the rural area, North Kodi; the most-detected pathogen was Ascaris lumbricoides, followed by Trichuris trichiura. Poly-parasitic intestinal infection was observed in more than one-third of infected children. Living in a rural area, lack of treatment with deworming drugs, use of a latrine without a septic tank, unclean water as the source of drinking water, no handwashing practice after defecation, and stunted children were the risk factors for intestinal parasitic infection observed in this study. We urge routine deworming every 6 months, providing clean water by building a drill well, and educating the community with good personal hygiene practice. Further study is currently ongoing to prove the efficacy of these comprehensive and holistic treatments in eradicating the parasitic infection. The scientific evidence obtained in this study will be recommended to local government as public policy.
Supplementary Materials
The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/tropicalmed8010045/s1, Supplementary Figure S1–S3 were taken from Google Earth©. Supplementary Figure S4–S6 were examined in the Laboratory of Malaria, Institute of Tropical Disease, Universitas Airlangga.
Author Contributions
I.S.S. was the principal investigator of the study. A.F.A., R.G.R., A.D., S.M.S. and K.V. participated in the study design. A.F.A. and A.D. supervised the data collection and analysis. S.B. and L.R. participated in the parasitology examination. I.S.S., A.F.A., A.D. and K.V. drafted the manuscript. All authors have read and agreed to the published version of the manuscript.
Funding
This study was funded by National Research Priority Scheme, Directorate General of Higher Education, Research and Technology, Ministry of Education, Culture, Research and Technology, Republic of Indonesia contract Number: 022/E4.1/AK.04.PRN/2021.
Institutional Review Board Statement
The study was conducted in accordance with the Declaration of Helsinki, and approved by the Ethics Committee of the Research Institute of YARSI University, Jakarta, Indonesia (No: 332/KEP-UY/BIA/X/2021, October 12, 2021, and registered at ClinicalTrials.gov with identifier number NCT05119218 for studies involving humans.
Informed Consent Statement
Informed consent was obtained from all subjects’ parents involved in the study.
Data Availability Statement
Not applicable.
Acknowledgments
The authors thank Ni Nyoman Metriani Nesa for assistance in the site coordination in Surabaya; Karolina Tallo for assistance in the site coordination in Kupang; and Novita Tjiang for assistance in the site coordination in North Kodi. We also thank Fitriah for assistance in the parasitology examination and Khadijah Rizky Sumitro for assistance in processing the data.
Conflicts of Interest
The authors declare no conflict of interest.
References
- Harhay, M.O.; Horton, J.; Olliaro, P.L. Epidemiology and Control of Human Gastrointestinal Parasites in Children. Expert Rev. Anti-Infect. Ther. 2010, 8, 219–234. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Osman, M.; El Safadi, D.; Cian, A.; Benamrouz, S.; Nourrisson, C.; Poirier, P.; Pereira, B.; Razakandrainibe, R.; Pinon, A.; Lambert, C.; et al. Prevalence and Risk Factors for Intestinal Protozoan Infections with Cryptosporidium, Giardia, Blastocystis and Dientamoeba among School Children in Tripoli, Lebanon. PLoS Negl. Trop. Dis. 2016, 10, e0004496. [Google Scholar] [CrossRef] [Green Version]
- Eyayu, T.; Kiros, T.; Workineh, L.; Sema, M.; Damtie, S.; Hailemichael, W.; Dejen, E.; Tiruneh, T. Prevalence of Intestinal Parasitic Infections and Associated Factors among Patients Attending at Sanja Primary Hospital, Northwest Ethiopia: An Institutional-based Cross-sectional Study. PLoS ONE 2021, 16, e0247075. [Google Scholar] [CrossRef]
- World Health Organization. Prevention and Control of Intestinal Parasitic Infections: Report of a WHO Expert Committee; World Health Organization: Geneva, Switzerland, 1987; pp. 1–86. [Google Scholar]
- Hajare, S.T.; Gobena, R.K.; Chauhan, N.M.; Eriso, F. Prevalence of Intestinal Parasite Infections and Their Associated Factors among Food Handlers Working in Selected Catering Establishments from Bule Hora, Ethiopia. BioMed Res. Int. 2021, 2021, 6669742. [Google Scholar] [CrossRef]
- Pullan, R.L.; Smith, J.L.; Jasrasaria, R.; Brooker, S.J. Global numbers of infection and disease burden of soil transmitted helminth infections in 2010. Parasites Vectors 2014, 7, 37. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Menteri Kesehatan Republik Indonesia. Peraturan Menteri Kesehatan Republik Indonesia Nomor 15 Tahun 2017 Tentang Penanggulangan Cacingan; Kementerian Kesehatan: Jakarta, Indonesia, 2017; pp. 1–78. [Google Scholar]
- Lee, J.; Ryu, J.S. Current Status of Parasite Infections in Indonesia: A Literature Review. Korean J. Parasitol. 2019, 57, 329–339. [Google Scholar] [CrossRef] [PubMed]
- Gizaw, Z.; Addisu, A.; Dagne, H. Effects of Water, Sanitation and Hygiene (WASH) Education on Childhood Intestinal Parasitic Infections in Rural Dembiya, Northwest Ethiopia: An Uncontrolled Before-and-after Intervention Study. Environ. Health Prev. Med. 2019, 24, 16. [Google Scholar] [CrossRef]
- Novitasari, N.A.; Fatah, M.Z. Systematic Review Of Risk Factor of Intestinal Parasite Infection. Media Gizi Kesmas 2021, 10, 165–179. [Google Scholar] [CrossRef]
- Onis, M.D.; Onyango, A.W.; Borghi, E.; Siyam, A.; Nishida, C.; Siekmann, J. Development of a WHO Growth Reference for School-aged Children and Adolescents. Bull. World Health Organ. 2007, 85, 660–667. [Google Scholar] [CrossRef]
- Maru, D.S. Prevalence of Intestinal Parasitic Infections and Associated Risk Factors among School Children in Adigrat town, Northern Ethiopia. Int. J. Emerg. Trends Sci. Technol. 2017, 04, 4943–4948. [Google Scholar] [CrossRef]
- Diarthini, N.L.P.E.; Swastika, I.K.; Ariwati, L.; Isyaputri, R.; Fitri, N.M.Y.; Hidajati, S.; Basuki, S. Blastocystis and Other Intestinal Parasites Infections in Elementary School Children in Dukuh Village, Karangasem District, Bali. Indones. J. Trop. Infect. Dis. 2018, 7, 57–61. [Google Scholar] [CrossRef] [Green Version]
- Else, K.J.; Keiser, J.; Holland, C.V.; Grencis, R.K.; Sattelle, D.B.; Fujiwara, R.T.; Bueno, L.L.; Asaolu, S.O.; Sowemimo, O.A.; Cooper, P.J. Whipworm and roundworm infections. Nat. Rev. Dis. Prim. 2020, 6, 44. [Google Scholar] [CrossRef] [PubMed]
- Centers for Disease Control and Prevention. Parasites-Soil-Transmitted Helminths. Available online: https://www.cdc.gov/parasites/sth/index.html#:~:text=Soil-transmittedhelminthsreferto,AncylostomaduodenaleandNecatoramericanus (accessed on 21 September 2022).
- World Health Organization. Soil-Transmitted Helminth Infections. Available online: https://www.who.int/news-room/fact-sheets/detail/soil-transmitted-helminth-infections (accessed on 21 September 2022).
- Wani, S.A.; Ahmad, F.; Zargar, S.A.; Dar, P.A.; Dar, Z.A.; Jan, T.R. Intestinal helminths in a population of children from the Kashmir valley, India. J. Helminthol. 2008, 82, 313–317. [Google Scholar] [CrossRef] [PubMed]
- Sungkar, S.; Ridwan, A.S.; Kusumowidagdo, G. The Effect of Deworming Using Triple-Dose Albendazole on Nutritional Status of Children in Perobatang Village, Southwest Sumba, Indonesia. J. Parasitol. Res. 2017, 2017, 5476739. [Google Scholar] [CrossRef] [Green Version]
- Lepper, H.C.; Prada, J.M.; Davis, E.L.; Gunawardena, S.A.; Hollingsworth, T.D. Complex Interactions in Soil-transmitted Helminth Co-infections from A Cross-sectional Study in Sri Lanka. Trans. R. Soc. Trop. Med. Hyg. 2018, 112, 397–404. [Google Scholar] [CrossRef] [PubMed]
- Statistics of Kupang Municipality. Kota Kupang Daya Dalam Angka (Kupang Municipality in Figures) 2021; Statistics of Kupang Municipality, Ed.; Statistics of Kupang Municipality: Kupang, Indonesia, 2021; pp. 1–22. [Google Scholar]
- Statistics of Sumba Barat Daya Regency. Kabupaten Sumba Barat Daya Dalam Angka (Statistics of Sumba Barat Daya in Figures) 2021; Statistics of Sumba Barat Daya Regency, Ed.; Statistics of Sumba Barat Daya Regency: Tambolaka, Indonesia, 2021; pp. 1–12, 31–44. [Google Scholar]
- Ojurongbe, O.; Oyesiji, K.F.; Ojo, J.A.; Odewale, G.; Adefioye, O.A.; Olowe, A.O.; Opaleye, O.O.; Bolaji, O.S.; Ojurongbe, T.A. Soil transmitted helminth infections among primary school children in Ile-Ife Southwest, Nigeria: A cross-sectional study. Int. Res. J. Med. Med. Sci. 2014, 2, 6–10. [Google Scholar]
- Shanan, S.; Abd, H.; Bayoumi, M.; Saeed, A.; Sandström, G. Prevalence of Protozoa Species in Drinking and Environmental Water Sources in Sudan. BioMed Res. Int. 2015, 2015, 345619. [Google Scholar] [CrossRef] [PubMed]
- Mane, A.B.; Reddy, N.S.; Reddy, P.; Chetana, K.V.; Nair, S.S.; Sriniwas, T. Differences of Hand Hygiene and its Correlates among School going Children in Rural and Urban Area of Karnataka, India. Arch. Med. 2016, 8. [Google Scholar] [CrossRef]
- Idowu, O.A.; Babalola, A.S.; Olapegba, T. Prevalence of soil-transmitted helminth infection among children under 2 years from urban and rural settings in Ogun state, Nigeria: Implication for control strategy. Egypt. Pediatr. Assoc. Gaz. 2022, 70, 5. [Google Scholar] [CrossRef]
- Darlan, D.M.; Winna, M.; Simorangkir, H.A.H.; Rozi, M.F.; Arrasyid, N.K.; Panggabean, M. Soil-transmitted Helminth and Its Associated Risk Factors Among School-aged Children. IOP Conf. Ser. Earth Environ. Sci. 2019, 305, 012066. [Google Scholar] [CrossRef]
- Apidechkul, T. Prevalence and Risk Factors of Intestinal Parasitic Infections among Hill Tribe School Children, Northern Thailand. Asian Pac. J. Trop. Dis. 2015, 5, 695–699. [Google Scholar] [CrossRef]
- Muslim, A.; Sofian, S.M.; Shaari, S.A.; Hoh, B.P.; Lim, Y.A.L. Prevalence, Intensity and Associated Risk Factors of Soil Transmitted Helminth Infections: A Comparison between Negritos (Indigenous) in Inland Jungle and Those in Resettlement at Town Peripheries. PLoS Negl. Trop. Dis. 2019, 13, e0007331. [Google Scholar] [CrossRef] [PubMed]
- Patterson, J.E.H.; Ruckstuhl, K.E. Parasite Infection and Host Group Size: A Meta-Analytical Review. Parasitology 2013, 140, 803–813. [Google Scholar] [CrossRef] [PubMed]
- Khan, W.; Khatoon, N.; Arshad, S.; Mohammed, O.B.; Ullah, S.; Ullah, I.; Romman, M.; Parvez, R.; Mahmoud, A.H. Evaluation of vegetables grown in dry mountainous regions for soil transmitted helminths contamination. Braz. J. Biol. 2022, 82, e238953. [Google Scholar] [CrossRef]
- Pino Santos, A.; Núñez Fernández, F.A.; Martínez Sánchez, R.; Domenech Cañete, I.; Rodríguez, M.; Jeres Puebla, L.; Rodríguez González, Z. Prevalence and Risk Factors for Intestinal Parasitic Infections in A Rural Community in “Consolación del Sur” Municipality, Cuba. West Indian Med. J. 2014, 63, 333–339. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nyantekyi, L.; Legesse, M.; Medhin, G.; Animut, A.; Tadesse, K.; Macias, C.; Degarege, A.; Erko, B. Community Awareness of Intestinal Parasites and The Prevalence of Infection among Community Members of Rural Abaye Deneba Area, Ethiopia. Asian Pac. J. Trop. Biomed. 2014, 4, S152–S157. [Google Scholar] [CrossRef] [Green Version]
- Subahar, R.; Susanto, L.; Astuty, H.; Winita, R.; Sari, I.P. Intestinal Parasitic Infections and Hemoglobin Levels among Schoolchildren participating in a Deworming Program in Jakarta, Indonesia: A Cross-sectional Study. Open Access Maced. J. Med. Sci. 2020, 8, 589–594. [Google Scholar] [CrossRef]
Figure 1.
Flow diagram of this study.
Figure 2.
Intestinal protozoan distribution in Kupang and North Kodi, East Nusa Tenggara; n = 30 children. Giardia lamblia was detected in a total of 13 children; Entamoeba coli was detected in a total of 6 children; Entamoeba histolytica was detected in a total of 1 child; Blastocystis spp. was detected in a total of 10 children (one child had ≥1 protozoan parasites).
Figure 2.
Intestinal protozoan distribution in Kupang and North Kodi, East Nusa Tenggara; n = 30 children. Giardia lamblia was detected in a total of 13 children; Entamoeba coli was detected in a total of 6 children; Entamoeba histolytica was detected in a total of 1 child; Blastocystis spp. was detected in a total of 10 children (one child had ≥1 protozoan parasites).
Figure 3.
Intestinal helminthic distribution in Kupang and North Kodi, East Nusa Tenggara; n = 51 children. Hymenolepis diminuta was detected in a total of 2 children; Trichuris trichiura was detected in a total of 28 children; Ascaris lumbricoides was detected in a total of 24 children; Hookworm was detected in a total of 1 child (one child had ≥1 helminthic parasites).
Figure 3.
Intestinal helminthic distribution in Kupang and North Kodi, East Nusa Tenggara; n = 51 children. Hymenolepis diminuta was detected in a total of 2 children; Trichuris trichiura was detected in a total of 28 children; Ascaris lumbricoides was detected in a total of 24 children; Hookworm was detected in a total of 1 child (one child had ≥1 helminthic parasites).
Figure 4.
Intestinal protozoan distribution in stunted and normal children in East Nusa Tenggara; n = 30 children. Giardia lamblia was detected in a total of 13 children; Entamoeba coli was detected in a total of 6 children; Entamoeba histolytica was detected in a total of 1 child; Blastocystis spp. was detected in a total of 10 children (one child had ≥1 protozoan parasites).
Figure 4.
Intestinal protozoan distribution in stunted and normal children in East Nusa Tenggara; n = 30 children. Giardia lamblia was detected in a total of 13 children; Entamoeba coli was detected in a total of 6 children; Entamoeba histolytica was detected in a total of 1 child; Blastocystis spp. was detected in a total of 10 children (one child had ≥1 protozoan parasites).
Figure 5.
Type of helminthic in stunted and normal children in East Nusa Tenggara; n = 51 children. Hymenolepis diminuta was detected in a total of 2 children; Trichuris trichiura was detected in a total of 28 children; Ascaris lumbricoides was detected in a total of 24 children; Hookworm was detected in a total of 1 child (one child had ≥1 helminthic parasites).
Figure 5.
Type of helminthic in stunted and normal children in East Nusa Tenggara; n = 51 children. Hymenolepis diminuta was detected in a total of 2 children; Trichuris trichiura was detected in a total of 28 children; Ascaris lumbricoides was detected in a total of 24 children; Hookworm was detected in a total of 1 child (one child had ≥1 helminthic parasites).
Table 1.
Univariate analysis of intestinal parasitic infection risk factors among children aged 36–45 months in Kupang and North Kodi, East Nusa Tenggara Timur, Indonesia.
Table 1.
Univariate analysis of intestinal parasitic infection risk factors among children aged 36–45 months in Kupang and North Kodi, East Nusa Tenggara Timur, Indonesia.
| Risk Factors | Intestinal Parasitic Infection | p Value * | OR (95% CI) | |
|---|---|---|---|---|
| Infected n (%) | Not Infected n (%) | |||
| Gender | 0.203 | 1.5 (0.8–2.8) | ||
| Boy | 33 (35.5) | 60 (64.5) | ||
| Girl | 28 (26.2) | 79 (73.8) | ||
| Locus | 0.0001 | 3.8 (2.0–7.4) | ||
| Rural area | 44 (44) | 56 (56) | ||
| Urban area | 17 (17) | 83 (83) | ||
| Family size | 0.171 | 2.1 (0.8–5.1) | ||
| >8 members | 10 (45.5) | 12 (54.5) | ||
| ≤8 members | 51 (28.7) | 127 (71.3) | ||
| Mother’s education (n = 198) | 0.094 | 2.1 (1.0–4.6) | ||
| Uneducated | 14 (45.2) | 17 (54.8) | ||
| Educated | 47 (28.1 | 120 (71.9) | ||
| Mother’s occupation (n = 194) | 0.609 | 1.3 (0.6–2.8) | ||
| Unemployed | 47 (31.1) | 104 (68.9) | ||
| Employed | 11 (25.6) | 32 (74.4) | ||
| Family income (n = 192) | 0.692 | 1.3 (0.6–2.7) | ||
| <Regional minimum wage | 45 (30.2) | 104 (69.8) | ||
| ≥Regional minimum wage | 11 (25.6) | 32 (74.4) | ||
| Low birth weight (n = 181) | 0.406 | 1.6 (0.7–3.5) | ||
| Yes | 11 (36.7) | 19 (63.3) | ||
| No | 41 (27.2) | 110 (72.8) | ||
| Deworming | 0.020 | 2.3 (1.2–4.4) | ||
| No | 23 (44.2) | 29 (55.8) | ||
| Yes | 38 (25.7) | 110 (74.3) | ||
| Type of sanitation facility | 0.0001 | 4.3 (2.0–9.2) | ||
| Latrine without septic tank | 21 (58.3) | 15 (41.7) | ||
| Latrine with septic tank | 40 (24.4) | 124 (75.6) | ||
| Source of drinking water | 0.0001 | 3.89 (2.0–7.8) | ||
| Unclean water | 24 (54.5) | 20 (45.5) | ||
| Clean water | 37 (23.7) | 119 (76.3) | ||
| Handwashing before eating | 0.671 | 1.3 (0.6–3.1) | ||
| No | 10 (35.7) | 18 (64.3) | ||
| Yes | 51 (29.7) | 121 (70.3) | ||
| Handwashing after defecation | 0.018 | 2.9 (1.3–6.6) | ||
| No | 14 (51.9) | 13 (48.1) | ||
| Yes | 47 (27.2) | 126 (72.8) | ||
| Stunted growth (n = 199) | 0.0001 | 3.4 (1.8–6.6) | ||
| Yes | 43 (43.0) | 57 (57) | ||
| No | 18 (18) | 82 (82) | ||
| Handwashing facility | 0.194 | 3.0 (0.8–11.6) | ||
| No | 5 (55.6) | 4 (44.4) | ||
| Yes | 56 (29.3) | 135 (70.7) | ||
| Total | 100 (50) | 100 (50) | ||
* Chi-squared test, significance set at p < 0.05.
Table 2.
Sociodemographic and hygiene practice characteristics of children aged 36–45 months from Kupang and North Kodi, East Nusa Tenggara Timur, Indonesia.
Table 2.
Sociodemographic and hygiene practice characteristics of children aged 36–45 months from Kupang and North Kodi, East Nusa Tenggara Timur, Indonesia.
| Variables | Kupang n (%) | North Kodi n (%) | p Value * |
|---|---|---|---|
| Gender | 0.442 | ||
| Boy | 51 (50.5) | 50 (50) | |
| Girl | 63 (55.8) | 50 (50) | |
| Family size | 0.473 | ||
| Small (<6 members) | 71 (62.3) | 55 (55) | |
| Medium (6–8 members) | 32 (28.1) | 31 (31) | |
| Large (>8 members) | 11 (9.6) | 14 (14) | |
| Mother’s education | 0.0001 | ||
| Uneducated | 4 (3.5) | 28 (28) | |
| Educated | 110 (96.5) | 72 (72) | |
| Mother’s occupation (n = 208) | 0.071 | ||
| Unemployed | 91 (56.9) | 69 (43.1) | |
| Employed | 20 (41.7) | 28 (58.3) | |
| Family income (n = 206) | 0.044 | ||
| <Regional minimum wage | 93 (58.5) | 66 (41.5) | |
| ≥Regional minimum wage | 19 (40.4) | 28 (59.6) | |
| Low birth weight (n = 195) | 1.000 | ||
| Yes | 18 (58.1) | 13 (41.9) | |
| No | 96 (58.5) | 68 (41.5) | |
| Deworming | 0.0001 | ||
| Yes | 107 (93.9) | 55 (55) | |
| No | 7 (6.1) | 45 (45) | |
| Source of drinking water | 0.0001 | ||
| Clean water | 114 (100) | 54 (54) | |
| Unclean water | 0 (0) | 46 (46) | |
| Type of sanitation facility | 0.0001 | ||
| Latrine with septic tank | 77 (67.5) | 18 (18) | |
| Latrine without septic tank | 37 (32.5) | 82 (82) | |
| Handwashing practice (before eating) | 0.0001 | ||
| Yes | 110 (96.5) | 76 (76) | |
| No | 4 (3.5) | 24 (24) | |
| Handwashing practice (after defecation) | 0.0001 | ||
| Yes | 112 (98.2) | 75 (75) | |
| No | 2 (1.8) | 25 (25) | |
| Handwashing facility | 0.014 | ||
| Yes | 113 (99.1) | 92 (92) | |
| No | 1 (0.9) | 8 (88.9) | |
| Height for age status | 0.187 | ||
| Stunted | 49 (43) | 52 (52) | |
| Normal | 65 (57) | 48 (48) | |
| Total | 114 (53.3) | 100 (46.7) |
* Chi-squared test, significance set at p < 0.05.
Table 3.
Socio-demographic and hygiene practice characteristics of stunted and normal children aged 36–45 months in East Nusa Tenggara Timur, Indonesia.
Table 3.
Socio-demographic and hygiene practice characteristics of stunted and normal children aged 36–45 months in East Nusa Tenggara Timur, Indonesia.
| Variables | Stunted n (%) | Normal n (%) | p Value * |
|---|---|---|---|
| Gender | 0.927 | ||
| Boy | 48 (47.5) | 53 (46.9) | |
| Girl | 53 (52.5) | 60 (53.1) | |
| Family size | 0.449 | ||
| Small (<6 members) | 63 (62.4) | 63 (55.8) | |
| Medium (6–8 members) | 18 (21.8) | 28 (36.3) | |
| Large (>8 members) | 20 (15.8) | 22 (8) | |
| Mother’s education level | 0.730 | ||
| Uneducated | 16 (15.8) | 16 (14.2) | |
| Educated | 85 (84.2) | 97 (85.8) | |
| Mother’s occupation (n = 208) | 0.909 | ||
| Unemployed | 77 (48.1) | 83 (51.9) | |
| Employed | 22 (45.8) | 26 (54.2) | |
| Family income (n = 206) | 0.834 | ||
| <Regional minimum wage | 76 (47.8) | 83 (52.2) | |
| ≥Regional minimum wage | 21 (44.7) | 26 (55.3) | |
| Low birth weight (n = 195) | 0.015 | ||
| Yes | 21 (67.7) | 10 (32.3) | |
| No | 69 (42.1) | 95 (57.9) | |
| Deworming | 0.017 | ||
| Yes | 93 (82.3) | ||
| No | 32 (31.7) | 20 (17.7) | |
| Source of drinking water | 0.036 | ||
| Clean water | 73 (72.3) | 95 (84.1) | |
| Unclean water | 28 (27.7) | 18 (15.9) | |
| Type of sanitation facility | 0.0001 | ||
| Latrine with septic tank | 30 (29.7) | 65 (57.5) | |
| Latrine without septic tank | 71 (70.3) | 48 (42.5) | |
| Handwashing practice (before eating) | 0.019 | ||
| Yes | 82 (81.2) | 104 (92) | |
| No | 19 (18.8) | 9 (8) | |
| Handwashing practice (after defecation) | 0.030 | ||
| Yes | 83 (82.2) | 104 (92) | |
| No | 18 (17.8) | 9 (8) | |
| Handwashing facility | 0.060 | ||
| Yes | 94 (45.9) | 111 (54.1) | |
| No | 7 (77.8) | 2 (22.2) | |
| Locus | 0.187 | ||
| Urban area | 49 (43) | 65 (57) | |
| Rural area | 52 (52) | 48 (48) | |
| Total | 114 (53.3) | 100 (46.7) |
* Chi-squared test, significance was set at p < 0.05.
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MDPI and ACS Style
Athiyyah, A.F.; Surono, I.S.; Ranuh, R.G.; Darma, A.; Basuki, S.; Rossyanti, L.; Sudarmo, S.M.; Venema, K. Mono-Parasitic and Poly-Parasitic Intestinal Infections among Children Aged 36–45 Months in East Nusa Tenggara, Indonesia. Trop. Med. Infect. Dis. 2023, 8, 45. https://doi.org/10.3390/tropicalmed8010045
AMA Style
Athiyyah AF, Surono IS, Ranuh RG, Darma A, Basuki S, Rossyanti L, Sudarmo SM, Venema K. Mono-Parasitic and Poly-Parasitic Intestinal Infections among Children Aged 36–45 Months in East Nusa Tenggara, Indonesia. Tropical Medicine and Infectious Disease. 2023; 8(1):45. https://doi.org/10.3390/tropicalmed8010045
Chicago/Turabian StyleAthiyyah, Alpha F., Ingrid S. Surono, Reza G. Ranuh, Andy Darma, Sukmawati Basuki, Lynda Rossyanti, Subijanto M. Sudarmo, and Koen Venema. 2023. "Mono-Parasitic and Poly-Parasitic Intestinal Infections among Children Aged 36–45 Months in East Nusa Tenggara, Indonesia" Tropical Medicine and Infectious Disease 8, no. 1: 45. https://doi.org/10.3390/tropicalmed8010045
