High Prevalence and Risk Factors for Hookworm and Strongyloides Stercoralis Infections in Rural East Kalimantan, Indonesia

Abstract

Background: Hookworm and Strongyloides stercoralis infections are neglected tropical diseases in developing countries, which have environmental risk factors with the potential for transmission of hookworm and S. stercoralis infections. This study aimed to explore the prevalence and risk factors for hookworm and S. stercoralis infections in East Kalimantan Province, Indonesia.

Methods: A cross-sectional study enrolled 213 participants from 28 villages, including 12 villages from Muara Kaman District and 16 villages from Marangkayu District in East Kalimantan Province. The data from 10-15 households of each village with 1-3 participants in each household were collected. In this study, Kato Katz and Koga agar plate cultures/KAP cultures were used for diagnosing hookworm and S. stercoralis infections among participants. The Pearson chi-square analysis was used to analyze the correlation between risk factors with hookworm and S. stercoralis infections.

Results: In this study, 72 (33.8%) and 17 (8.0%) participants were infected with hookworm and S. stercoralis, respectively. The prevalence of hookworm infection reported was higher than S. stercoralis infection in rural areas of East Kalimantan Province. Hookworm infection has been significantly associated with demographic factors, sanitation conditions and personal hygiene. In addition, high hookworm infection has been significantly associated with environmental factors such as locality of district, organic carbon content in the soil, temperature, humidity, number of days of rainfall, volume of rainfall, wet/dry soil around houses, and habitation. However, S. stercoralis infection has not been significantly correlated with demographic factors, sanitation conditions, and personal hygiene. The highest odds ratio of hookworm infection was in village areas surrounded by a river or coastal areas OR: 2.92 (95% CL: 1.38-6.24), while the highest odds ratio of S. stercoralis infection was in households with habitation with humans infected with S. stercoralis OR: 95% CL: 8.33 (2.27-30.61).

Conclusions: The high prevalence and risk factors of hookworm and S. stercoralis infections in rural communities in East Kalimantan Province. Characteristics of demographic factors, sanitation conditions, and personal hygiene that were correlated with hookworm and S. stercoralis infection should be used for control and prevention programs to reduce hookworm and S. stercoralis infections, especially in rural areas.

Background

Hookworm and Strongyloides stercoralis are two soil-transmitted helminths (STH) that are highly prevalent infections and serious public health concerns globally. Hookworm causes the highest public health burden among STH, while S. stercoralis causes long-lasting infections and significant morbidity. These two parasites are highly prevalent in poor rural communities in tropical and subtropical areas in many developing countries (1). They are transmitted through unprotected contact with soil that is endemic in tropical and temperate regions. In 2010, the prevalence of hookworm infection and S. stercoralis infection was estimated in 438.9 million people and 100 million people, respectively. Almost 70% of these infections occurred in Asia (2–4). Humans acquire hookworm and S. stercoralis infections through direct skin contact with infective third-stage larvae, where soil that was contaminated by human feces penetrate the intact human skin and eventually reach the small intestine (5). Generally, hookworm and S. stercoralis infections are found among poor people with poor environmental sanitation and where the climate is warm and humid (6, 7).

Factors affecting the difference in the prevalence of hookworm infection and S. stercoralis infection may include good hygiene practices among the population, availability of a sewage system, and length of the rainy season. Environmental factors have contributed to the transmission of diseases as well as to the growth and development of the worms (8, 9). Environmental factors, especially the long rainy season, may affect the decrease in the prevalence of S. stercoralis infection but not hookworm infection. A previous study demonstrated that the prevalence of S. stercoralis infection in Southern Thailand is lower than in other parts of the country. However, the prevalence of hookworm infection is still high in Southern Thailand because of the 10-months-long rainy season in Southern Thailand in contrast with the 4-months-long rainy season in other parts (10). Another study in Cambodia reported a lower prevalence of S. stercoralis infection in the areas with heavy rainfall than in low rainfall areas, where the high amount of the organic carbon content in the soil affects the lower prevalence of S. stercoralis infection (11). A previous study in Southern Laos demonstrated hookworm infection and S. stercoralis infection at about 56.1% and 41%, respectively (12).

Kutai Kertanegara Regency, East Kalimantan Province, Indonesia is located at 0.44019⁰S and 116.98139⁰E. The average temperature is 28⁰C (26-32⁰C). Muara Kaman District is located at the surrounding Mahakam River and is close in proximity with forest areas and palm plantations. In contrast, Marangkayu District is located in a coastal area and surrounded by rubber plantations, palm plantations, and rice fields. We collected data from 28 villages, consisting of 12 villages from Muara Kaman District and 16 villages from Marangkayu District. The prevalence of hookworm and S. stercoralis infections in rural East Kalimantan Province, Indonesia, remains unclear. Because the environment is suitable for hookworm and S. stercoralis infections in this area, it is important to determine the prevalence and risk factors for these two parasites. This study aimed to explore the prevalence and risk factors (including soil quality, surrounding vegetation, temperature, humidity, village areas, length of rainy season, type of pets (cats or dogs), personal hygiene, and sanitation conditions of households) for hookworm and S. stercoralis infections in East Kalimantan Province, Indonesia.

Methods

Study design

This cross-sectional study was conducted from July 2018 to September 2019 in rural areas of Muara Kaman District and Marangkayu District, Kutai Kertanegara Regency, East Kalimantan Province, Indonesia. Data was collected from 10–15 households in each village with 1–3 participants in each household. The demographic data was collected from 213 participants and was analyzed with the environmental factors (13).

Study population, sample size, and sampling technique

Two districts in Kutai Kertanegara Regency, East Kalimantan Province, were selected for the purpose of this study: Muara Kaman District and Marangkayu District (Fig. 1), where these areas have differences in soil quality, number of days and yearly volume of rainfall, temperature, humidity, elevation above sea level, village areas, and surrounding vegetation. These areas were selected based on the potential risk of hookworm and S. stercoralis infections due to the following characteristics: rural areas, poor sanitation and hygiene practices, agricultural activity, and surrounding forests. The sample size was calculated using a prevalence rate (p) of 55.4% as detailed from a previous study (23), with a 95% confidence interval (z = 1.96) and a 10% margin of error (d = 0.1). Therefore, the calculated sample size was 95 participants per district. However, the final sample size would end up being reduced by around 15% due to subjects being unable to pass stool on the study date. Thus, the aim was for a sample size of 110 participants per district. A simple random sampling method was used to select the population from each district. Inclusion criteria for participants included the following: ≥2 years old, lived in both areas, and were able to complete questionnaires and provide stool samples. One hundred and ten participants per area were randomly selected and were given the instructions, and they were also provided the questionnaires and plastic containers for stool sample collection. In total, 220 participants were enrolled and completed the questionnaires. Seven participants were excluded from the study because they did not send in their stool samples. In total, 213 participants were included for this study.

Data collection and laboratory processing

The stool samples were collected and sent to The Biomedical Laboratory, School of Public Health, Mulawarman University. Two methods were performed to identify the parasites including agar plate culture and the Kato-Katz technique. A modified agar plate culture was performed as described by Koga et al., 1991. Briefly, approximately 2 grams of stool sample was placed at the center of nutrient agar and kept at room temperature for five days. Tracks from larva crawling and larvae or adult worms were observed under an inversed microscope. If any tract was spotted, 10 ml of 10% formalin was added to the agar surface for 5–10 minutes and transferred to a centrifuged tube. Centrifugation of suspension was performed at 2,500 rpm for 5 minutes, and then the supernatant was discarded. The sediment was further examined for hookworm and S. stercoralis larvae or adult worms. For the Kato-Katz thick smear, 50 mg of stool was placed on a slide and covered with a cellophane paper soaked in glycerin solution for 24 hours. The stool was spread out using a rubber stick and examined after 30 minutes, and the eggs of parasites were counted (14–16). The environmental conditions of houses surrounding the village were recorded on the same day or following the day after stool samples were collected.

Data analysis

Results

Discussion

The prevalence of hookworm infections showed higher than in S. stercoralis infections in rural East Kalimantan, Indonesia. In this study, we found that the prevalence of hookworm infection was higher in Muara Kaman District than in Marangkayu District, while the prevalence S. stercoralis infection was higher in Marangkayu District than in Muara Kaman District. The difference in environmental factors between Muara Kaman District and Marangkayu District was that Muara Kaman District is surrounded by palm plantations and river area, which might affect the increasing or decreasing prevalence of S. stercoralis infection in rural areas (2). A similar study was performed in Manufahi District, Timor Leste, with a prevalence of hookworm infection at 62.8% (17).

In regard to the organic carbon content in the soil, hookworm infection was higher in the category > 2.47–4.04% than in the category 1.37–2.47% with prevalence at 51 (41.8%) and 21 (23.1%), respectively. S. stercoralis infection was higher in the category 1.37–2.47 than in the category > 2.47–4.04% with prevalence at 13 (14.3%) and 4 (3.3%), respectively. The organic carbon content in the soil with the category > 2.47–4.04% was 1.70 times more likely for hookworm infection than in the category 1.37–2.47%, while the organic carbon content in the soil with the category 1.37–2.47% was 2.56 times more likely for S. stercoralis infection than in the category > 2.47–4.04%. A Cambodian study explained that high amounts of organic carbon content in the soil might not affect the prevalence of hookworm infection but might affect the prevalence of S. stercoralis infection (11). This may indicate that the organic carbon content in the soil in East Kalimantan Province might not reduce hookworm infection but might reduce S. stercoralis infection. From the study of Sebastian H, et al., the organic carbon content in the soil had an indirect effect on nematodes, but the effect of the organic carbon content via food organisms was usually on the abundance, cell size, and activity of bacteria (Escherichia coli) (18). Absorption of organic carbon by bacterial cells, serving as food for the nematodes, may be an important factor for the availability of organic carbon for hookworm.

The present study demonstrated that hookworm infection was associated with temperature, humidity, number of days of rainfall, rainfall volume, and elevation above sea level. These results were supported by a previous study that demonstrated that the rainy season may reduce the prevalence of hookworm and S. stercoralis infections (10). Another previous study also supported the results of this study by demonstrating that elevation contributed to the distribution of the prevalence hookworm and S. stercoralis infections (19). Environmental factors in East Kalimantan Province might be similar to Southern Thailand including long rainy seasons, temperature, and several geographical characteristics, which might have an impact on the higher prevalence of hookworm infection in East Kalimantan Province than in Southern Thailand (10). Another study in Southern Laos demonstrated a high prevalence of S. stercoralis infection during heavy rainfall with poor sanitation (12).

Hookworm infection was higher in households surrounded by vegetation and villages surrounded by palm plantations and/or rubber plantations than in villages surrounded by rice fields with the prevalence at 65 (38.9%) and 7 (15.2%), respectively; while S. stercoralis infection was higher in villages surrounded by rice fields than those surrounded by palm plantations and/or rubber plantations with the prevalence at 5 (10.9%) and 12 (7.2%), respectively. The reason is because the surrounding palm plantations have a higher temperature than the rice fields, which provide a suitable environment for hookworm but not for S. stercoralis. In addition, the soil covering at palm plantations might be a potential source for hookworm transmission rather than S. stercoralis infection, whereas rice fields might be a potential source for S. stercoralis infection during farming activity (20).

The prevalence of hookworm infection was higher in village areas with a river or coastal areas than in hill areas, while the prevalence of S. stercoralis infection was higher in hill areas. In addition, hookworm infection was more likely in houses surrounded by wet soil rather than dry soil, while S. stercoralis infection was more likely in houses surrounded by dry soil rather than wet soil. Hookworm and S. stercoralis infections were more likely in participants who have dogs than those who do not have dogs. Dogs were a potential risk of transmitting hookworm and S. stercoralis among communities in rural villages with poor sanitation and a low quality of personal hygiene among members of the household. The results of this study were supported by a similar research conducted among Cambodian participants, where dogs were a serious risk factor for hookworm and S. stercoralis infections. Moreover, a previous study also demonstrated that dogs have a higher potential risk for hookworm and S. stercoralis infection than cats (21, 22). A study in Southern Thailand also demonstrated that dogs were correlated with hookworm and S. stercoralis infections (23). The factors related to the risk of hookworm and S. stercoralis infections consisted of poor hygiene, including infrequent hand washing and unclean feet after soil contact. These factors supported the penetration of S. stercoralis larvae to the human host (23, 24).

Conclusions

The prevalence of hookworm infection was higher than S. stercoralis infection in rural areas of East Kalimantan Province. The higher prevalence of hookworm infection than S. stercoralis infection might be due to environmental factors, sanitation conditions, and personal hygiene of the participants. Environmental factors such as the quality of the soil, length of rainy season, surrounding vegetation, and village areas were significant factors for increasing hookworm infection. In contrast, some of these factors became preventative factors for the prevalence of S. stercoralis infection. Demographic characteristics, sanitation conditions, and personal hygiene that were correlated with hookworm and S. stercoralis infections should be used for the control or reduction of hookworm and S. stercoralis infections in the rural areas of East Kalimantan Province.

List of abbreviations

S. stercoralis; Strongyloides stercoralis, OR; odds ratio, STH; soil-transmitted helminthes.

Declarations

Ethical approval and consent to participate

The study protocol was approved by the Ethical Clearance Committee on human rights related to research involving human subjects, Walailak University (HE: No. WUEc-18-034-01).

Consent for publication

Official permission and ethical clearance for collection of human fecal samples were obtained from the head of the village and the head of the household.

Availability of supporting data

All data related to the present study in this manuscript are available.

Competing interests

The authors declare that there is no conflict of interest regarding the publication of this article.

Funding

This work was supported by a grant from Walailak University (Contract No. 17/2561) and a grant for PhD studies from the East Kalimantan Provincial Government, Indonesia.

Authors’ contributions

All authors conceived of the idea and participated in the design of this study. BS, JT, and MK conducted the study. BS, SW, SP, WA, and JT were responsible for the interpretation of the results, drafting of the manuscript, and reading for intellectual content. All authors read and approved the final manuscript.

Acknowledgments

We are grateful to the participants and local authorities of Muara Kaman District and Marangkayu District, East Kalimantan Province, Indonesia. We would like to deeply thank the Dean of the School of Allied Health, Walailak University, and the Dean of the School of Public Health, Mulawarman University, for permitting us to use their laboratory and for supporting us through an approval letter for this research.

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