ABSTRACT.
Khong Chiam is located on the border between Thailand and Laos, with the Mekong River as a natural barrier. The main river, Mun, also flows through Khong Chiam to meet the Mekong River, making Khong Chiam a community that primarily relies on water for agriculture and fisheries. A variety of intestinal parasites are endemic in Khong Chiam. A survey of 1,423 residents from 35 villages located along the Mun and Mekong Rivers in Khong Chiam was conducted from April 2021 to April 2022. Stool examination using a modified formalin–ether concentration technique revealed a 10.2% prevalence of various intestinal helminth and protozoan infections. Single infections with Strongyloides stercoralis (46/1,423; 3.2%), Opisthorchis viverrini (40/1,423; 2.8%), and Taenia spp. (22/1,423; 1.5%) were predominant. Most helminth infections were of low intensity. Intestinal parasitic infections (IPIs) were more prevalent in males than in females, except for opisthorchiasis, which was equally prevalent in both sexes. Questionnaire interviews with the voluntary participants revealed that factors including age, comorbidity, previous infection with intestinal parasites, and anthelmintic drugs used in the past year were statistically related to the IPI status of the participants. The interviews revealed inadequate hygiene practices; lack of knowledge; inaccurate perceptions about health, IPI, and cholangiocarcinoma; and low intention to prevent IPI among participants. However, providing education and accurate information has been shown to raise awareness and reduce the risk of IPI. Stool examinations, drug treatment, and the promotion of individual self-prevention through sanitary behaviors are important for the control of IPI in this endemic area.
INTRODUCTION
Several parasites are endemic to many of the countries in the lower Mekong Basin. Many variables, including tropical temperature and geography, the presence of natural hosts, and the unsanitary behavior of villagers, contribute to the maintenance of parasitic lifecycles in this region, and many villagers remain at risk of infections.
Many provinces in northeastern Thailand continue to report a high prevalence of intestinal parasitic infections (IPIs), particularly opisthorchiasis, which is predominant in many populations. In addition, strongyloidiasis also exhibits a high prevalence in many areas of the northeast. The prevalence of IPIs, particularly opisthorchiasis and strongyloidiasis, have also been reported in immigrant workers working in northeastern Thailand. Intestinal parasitic infections in immigrant workers have raised hygiene concerns related to the potential spread of intestinal parasites in environmental reservoirs. Furthermore, male sex, older age, and raw food-consuming habits have been found to be the risk factors that contribute to IPI in these populations.1–5
Although parts of northeast Thailand have been urbanized, and residents are more educated and have easier access to various forms of information from the media, they continue to engage in traditional lifestyles and consume raw foods, resulting in the continued prevalence of IPI. In addition, many areas in northeastern Thailand remain rural and remote, and the residents of these areas are neglected.
Khong Chium is the easternmost district in Ubon Ratchathani Province. The east side of Khong Chiam is bordered by the Mekong River, which is a natural barrier between Thailand and the Lao People’s Democratic Republic. Therefore, crossing the Mekong River by boat via temporary checkpoints for various purposes, such as tourism, employment, medical services, marriage, and visiting relatives, is common in the populations of these two countries. As such, there are ∼1,148 non-Thai people living in Khong Chiam (according to the Ubon Ratchathani Provincial Statistical Annual Report 2021, Ubon Ratchathani Provincial Statistical Office, Ministry of Digital Economy and Society). Khong Chiam is also the point where the Mun River, which flows through several northeastern provinces, meets the Mekong River. Therefore, several villages in Khong Chiam along the Mun and Mekong Rivers are water-based communities. Furthermore, the similarity of the culture, traditions, and lifestyles between the Thai and Lao people along the Mekong River has led to similar occupations related to agriculture, fishing, and the tradition of consuming raw food. Additionally, Khong Chiam has many areas that remain remote, rural, and neglected. The tropical climate and abundance of natural hosts in Khong Chiam support the possibility of parasite endemicity in this border area. Nevertheless, there is a lack of information regarding the prevalence and risk factors of parasitic infections.
With this survey, we aimed to investigate the prevalence and risk factors of IPI among residents of Khong Chiam. The demographic information of the residents, as well as their knowledge and perceptions regarding IPI and cholangiocarcinoma (CCA), were determined through questionnaire-based surveys. Basic information on the prevalence of IPI and its relationship with various influencing factors can assist in improving our understanding of the situation and trends in IPI in this area, which is critical for future prevention and control planning.
MATERIALS AND METHODS
Study area and population.
A cross-sectional survey of intestinal helminth and protozoan infections was conducted on individual villagers in 35 villages served by the eight health promotion hospitals in the Khong Chiam District of Ubon Ratchathani Province from April 2021 to April 2022. The survey began with the research assistant organizing a meeting with the villagers at the community hall to inform them about the goals, methods, potential risks, and benefits of the study. The research assistant also briefed the villagers in the local language about the participant information sheet and the need to obtain written consent and fecal samples, as well as the potential for them to be asked to complete the questionnaire.
After this announcement, 1,596 people enrolled in the survey. Each participant read the information sheet and provided written informed consent for themselves or for their child before the fecal samples were submitted and the questionnaire interviews were conducted. For illiterate participants, the research assistant read the informed consent form aloud and approved the signatures, which were provided via a fingerprint. A witness observed all the procedures associated with the signing of the consent form.
Stool examination for parasitic infection.
All participants received advice on fecal collection from a research assistant. Each participant received a parasitology kit that was distributed to villagers by village health volunteers. The kit included a screw-cap container labeled with a name and code, a spoon, and an instruction sheet. The participants sent a fecal sample of ∼2 g to the community hall in the village within 3 days of receiving the kit. Fecal samples were transported daily on ice to the laboratory of the College of Medicine and Public Health at Ubon Ratchathani University and were prepared by using a modified formalin–ether concentration technique (M-FECT).6
Briefly, the M-FECT method involved suspending 2 g of feces in 10 mL of normal saline and then filtering it through two layers of gauze into a 15 mL conical tube. The samples were then centrifuged at 2,000 rpm for 2 minutes to collect the fecal sediment. The fecal sediment was washed multiple times with normal saline until the supernatant became clear. The fecal sediment was resuspended in 7 mL of 10% formalin and 3 mL of ethyl acetate to remove fat and debris. The mixture was vigorously shaken for 10 minutes before centrifugation. The layer of debris and fat was then removed using an applicator stick, and the liquid was decanted. Residual debris and liquid in the tube were removed by using a gauze swab. The fecal sediment was retrieved and resuspended in 1 mL of 10% formalin. The total number of drops was counted, and two drops of fecal sediment were examined under a light microscope. Medical technicians from Ubon Ratchathani University Hospital, who were not informed about the health status or other details of the study participants, conducted the stool examinations. Helminth eggs, larvae, and cysts were investigated. The number of eggs was counted to calculate the number of eggs per gram (EPG) in the feces and to evaluate the intensity of the infection. The codes for positive cases were recorded, and the infection prevalence was calculated.
Participants who were diagnosed with intestinal helminth and protozoan infections were informed individually and offered drug treatment, depending on the class of parasite, by qualified clinicians from Ubon Ratchathani University Hospital. The antiparasitic drugs administered to infected participants included a single dose of praziquantel for fluke (opisthorchiasis; 40 mg/kg)7,8 and tapeworm (Taenia) infections (10 mg/kg),9,10 as well as albendazole (400 mg tablet, single dose) for hookworms11 and strongyloidiasis (800 mg/day for 3 days).12 Metronidazole (15 mg/kg) was administered three times a day for 5 days for giardiasis.13 Infection with Entamoeba coli was not an indication for drug treatment.
Geographical analysis.
The geographic coordinates of the houses of infected participants were recorded by using a global positioning system device. These geographical data were analyzed by using a geographic information system to map points corresponding to the locations of the infected villagers’ houses. Various colored spots were generated to indicate infection with different genera and species of intestinal parasites.
Questionnaire survey.
Participants identified as having IPIs and a sample of those without IPIs were invited to complete the questionnaire survey to provide general personal and demographic information, knowledge, and health perceptions associated with IPI and CCA. The questionnaire used in this survey was adapted from the questionnaire on diseases and health problems from the Center for Disease Control in Ubon Ratchathani Province. Questionnaire interviews were performed independently at health-promoting hospitals by trained interviewers in the local language and translated into English. The questionnaire was pretested before the interviews with 10 villagers who were not involved in the current study to ensure appropriate content and language.
The questionnaire included demographic information such as age, sex, body mass index (BMI), education level, occupation, and monthly income. The questionnaire also included questions that were reported as yes or no to assess comorbidities, animal raising and feeding, defecation hygiene, previous screening for parasitic infection, and the use of anthelmintic drugs. Furthermore, the questionnaire included 25 statements divided into five sections to assess knowledge and health perceptions of IPI, CCA, and factors that promote good hygiene.
The first section contained seven statements that focused on the risk of IPI from consuming raw and unclean foods, as well as poor personal hygiene practices. The eight statements in the second section were used to examine perceptions regarding the safety and efficacy of anthelmintic drugs in treating IPI, as well as the perception of the severity of opisthorchiasis and maintaining good health through the consumption of nutritious foods. In the third section, through five statements, the questions assessed participants’ knowledge of CCA, including the risk of reinfection with Opisthorchis viverrini (O. viverrini), the presence of carcinogens in fermented foods, and the risk of carcinogens in CCA development. The views of the respondents regarding avoiding CCA by discontinuing the consumption of raw freshwater fish, as well as their attention to opisthorchiasis treatment, were also investigated in the third section. The respondents’ perceptions of the occurrence of CCA were determined in the fourth section. The final section included three statements designed to determine the factors that promote good personal hygiene practices for staying healthy and avoiding CCA. Some statements in the interview questionnaire were negatively keyed, indicating that the disagreement or falsity was correct, and these items were scored in reverse.
STATISTICAL ANALYSES
The fecal examination results were entered into a Microsoft Excel (Microsoft Corp., Redmond, WA) spreadsheet and presented as a percentage, as well as the intensity of each parasite. The interview data were analyzed by using Stata Statistical Software version 18.0. (StataCorp, College Station, TX). Categorical data are presented as numbers and percentages to represent the trends of the target group. Binary logistic regression analysis was used to determine the independent effects of the variables by calculating the strength of the association between the IPI score and associated factors using odds ratios (ORs) and 95% CIs. Statistical significance was set at P <0.05. The ORs and 95% CIs were also used to assess which knowledge and health perceptions of the respondents were risk factors for IPI.
RESULTS
Parasitology.
After registering to join the study, 1,423 participants provided stool samples for IPI examination, representing a participation rate of 89.2%. Stool examination revealed a 10.2% prevalence of helminth and protozoan infections in the villagers of Khong Chiam (145 participants; 96 males and 49 females). The primary infection was a single infection with one of nine species of intestinal parasites, including Strongyloides stercoralis (S. stercoralis; 46; 3.2%), O. viverrini (40; 2.8%), Taenia spp. (22; 1.5%), hookworm (7; 0.5%), Giardia lamblia (G. lamblia; 7; 0.5%), Enterobius vermicularis (1; 0.1%), Echinostoma spp. (1; 0.1%), and Trichuris trichiura (1; 0.1%), as well as infection with a nonpathogenic amoeba, Entamoeba coli (7; 0.5%; Table 1).
Table 1.
Prevalence of intestinal helminths and protozoa infection among participants from Khong Chiam
| Type of Intestinal Parasitic Infection | Males | Females | Total | Percentage |
|---|---|---|---|---|
| Helminths | ||||
| Strongyloides stercoralis | 38 | 8 | 46 | 3.2 |
| Opisthorchis viverrini | 20 | 20 | 40 | 2.8 |
| Taenia spp. | 14 | 8 | 22 | 1.5 |
| Hookworm | 5 | 2 | 7 | 0.5 |
| Enterobius vermicularis | 0 | 1 | 1 | 0.1 |
| Echinostoma spp. | 0 | 1 | 1 | 0.1 |
| Trichuris trichiura | 1 | 0 | 1 | 0.1 |
| Protozoa | ||||
| Entamoeba coli | 4 | 3 | 7 | 0.5 |
| Giardia lamblia | 6 | 1 | 7 | 0.5 |
| Mixed infections | ||||
| Strongyloides stercoralis, Opisthorchis viverrini | 3 | 2 | 5 | 0.3 |
| Strongyloides stercoralis, hookworm | 3 | 1 | 4 | 0.3 |
| Strongyloides stercoralis, Giardia lamblia | 1 | 0 | 1 | 0.1 |
| Strongyloides stercoralis, Taenia spp., hookworm | 0 | 1 | 1 | 0.1 |
| Taenia spp., Echinostoma spp. | 1 | 0 | 1 | 0.1 |
| Opisthorchis viverrini, Taenia spp. | 0 | 1 | 1 | 0.1 |
Double-infections with S. stercoralis and various intestinal parasites, including O. viverrini (5; 0.3%), hookworm (4; 0.3%), and G. lamblia (1; 0.1%), and double-infections with Taenia spp. and O. viverrini (1; 0.1%) and Echinostoma spp. (1; 0.1%) were also identified, as were triple-infections with S. stercoralis, Taenia spp., and hookworm (1; 0.1%; Table 1). The residential distribution of the intestinal parasite-infected participants in this survey is demonstrated on the Khong Chiam District map (Figure 1).
Figure 1.
Distribution of IPI in participants from Khong Chiam.
The age of the participants infected with the parasites ranged between 14 and 83 years, with a median age of 55 years. Intestinal parastic infection in males was most frequently detected at age 51–60 years of age, with a median age of 55 years, whereas infected females were mostly 41–50 years of age, with a median age of 45 years.
Intestinal helminth and protozoan infections were more prevalent in males than females, except for opisthorchiasis, which was equally prevalent in both sexes. The highest prevalence of opisthorchiasis in females was found at 41–50 years of age, and in males, it was most prevalent at 51–60 years of age. In addition, opisthorchiasis was detected in a young boy from Khong Chiam.
The intensity of helminth infection was calculated based on the number of EPG and classified as described by Laymanivong et al.14 The survey participants with opisthorchiasis primarily had mild infections. Only five participants with opisthorchiasis, both males and females aged 41–50 years, had moderate infections. Male and female participants with opisthorchiasis who had mixed infections with Taenia spp. (n = 1) and S. stercoralis (n = 4) had light-intensity infections.
Participants with other intestinal helminth infections, including hookworms, enterobiasis, trichuriasis, and echinostomiasis, also had mild infections. Only one participant with hookworm infection had moderate-intensity infection.
Questionnaire survey.
The standardized questionnaire was used to collect data on several aspects that influenced intestinal helminth and protozoan infections in participants. Responses were completed by 104/145 participants diagnosed with IPI (60 males and 44 females; 71.7% participation rate) and 104 participants who were not infected with intestinal parasites (50 males and 54 females).
General characteristics and demographic information.
Responses were collected from 104 participants with IPI who were diagnosed with strongyloidiasis (n = 41), opisthorchiasis (n = 34), taeniasis (n = 15), hookworm infection (n = 4), and other infections with protozoa and intestinal flukes (n = 10). Respondents from the infected and noninfected groups were interviewed to obtain general characteristics and demographic information (Table 2). The ages of the infected respondents, mainly 41–60 years, were higher than those of the noninfected respondents, who were mostly younger than 40 years.
Table 2.
General characteristics and demographic information of participants diagnosed with intestinal parasitic infection
| Demographic Characteristics | Category | Number of Parasite-Infected Respondents (%) | Number of Non-Parasite Infected Respondents (%) | OR | 95% CI | P-Value |
|---|---|---|---|---|---|---|
| Sex | Males | 60 (57.7) | 50 (48.1) | 1.00 | – | – |
| Females | 44 (42.3) | 54 (51.9) | 0.67 | 0.39 to 1.17 | 0.164 | |
| Age | ≤40 | 9 (8.7) | 59 (56.7) | 1.00 | – | – |
| 41–60 | 72 (69.2) | 44 (42.3) | 2.37 | 1.57 to 3.16 | <0.001 | |
| ≥61 | 23 (22.1) | 1 (1) | 5.01 | 2.89 to 7.13 | <0.001 | |
| BMI | Obesity | 8 (7.7) | 4 (3.8) | 0.52 | 0.21 to 1.31 | 0.168 |
| Overweight | 23 (22.1) | 12 (11.5) | 1.32 | 0.44 to 3.98 | 0.614 | |
| Normal weight | 60 (57.7) | 79 (76) | 1.38 | 0.31 to 6.02 | 0.665 | |
| Underweight | 13 (12.5) | 9 (8.7) | 1.00 | – | – | |
| Education | Illiterate | 9 (8.7) | 5 (4.8) | 1.00 | – | – |
| Elementary | 69 (66.3) | 87 (83.7) | 0.44 | 0.14 to 1.37 | 0.158 | |
| High school and higher | 26 (25) | 12 (11.5) | 1.20 | 0.33 to 4.37 | 0.778 | |
| Occupation | Unemployed | 9 (8.7) | 1 (1) | 1.00 | – | – |
| Self-employed | 12 (11.5) | 10 (9.6) | 0.13 | 0.014 to 1.23 | 0.077 | |
| Student | – | – | – | – | – | |
| Farmer/gardener | 71 (68.3) | 83 (79.8) | 0.09 | 0.11 to 0.76 | 0.027 | |
| Fisherman | 7 (6.7) | 5 (4.8) | 0.15 | 0.01 to 1.65 | 0.123 | |
| Merchant | 5 (4.8) | 5 (4.8) | 0.11 | 0.01 to 1.23 | 0.074 | |
| Income/month ($)* | <30 | 19 (18.2) | 16 (15.4) | 1.00 | – | – |
| 30–150 | 50 (48.1) | 56 (53.8) | 0.75 | 0.35–1.61 | 0.466 | |
| 150–300 | 27 (26) | 25 (24) | 0.90 | 0.38–2.14 | 0.829 | |
| >300 | 8 (7.7) | 7 (6.7) | 0.96 | 0.28–3.23 | 0.951 | |
| Comorbidity | No | 34 (32.7) | 90 (86.5) | 1.00 | – | – |
| Yes (gout, hypertension, diabetes, colon cancer, allergy, cerebral vascular obstruction, a mix of comorbidities: gout and hypertension) | 70 (67.3) | 14 (13.5) | 13.23 | 6.59 to 26.55 | <0.001 | |
| Animal raising | No | 48 (46.2) | 22 (21.2) | 1.00 | — | — |
| Pets (cats and dogs) and livestock (cows and buffalos) | 56 (53.8) | 82 (78.8) | 0.31 | 0.17 to 0.57 | <0.001 | |
| Feeding animals with leftover food from household | No | 12 (11.5) | 16 (15.4) | 1.00 | – | – |
| Yes | 92 (88.5) | 88 (84.6) | 1.39 | 0.62 to 3.11 | 0.428 | |
| Use toilet | No | 0 | 0 | – | – | – |
| Yes | 104 | 104 | – | – | – | |
| Previous stool examination in the past year | No | 71 (68.3) | 80 (76.9) | 1.00 | – | – |
| Yes, with a negative parasite | 14 (13.4) | 19 (18.3) | 0.83 | 0.38 to 1.77 | 0.632 | |
| Yes, with positive parasites | 19 (18.3) | 5 (4.8) | 4.28 | 1.51 to 12.06 | 0.006 | |
| Previous anthelmintic drugs used in the past year | No | 24 (23.1) | 59 (56.7) | 1.00 | – | – |
| Yes | 80 (76.9) | 45 (43.3) | 4.37 | 2.40 to 7.95 | <0.001 |
BMI = body mass index; OR = odds ratio.
According to the U.S. dollar-to-That bhat exchange rate as of November 1, 2021.
Logistic regression analysis revealed that age was a significant factor in the occurrence of IPI. The interview showed that the older respondents, particularly those aged 41–60 years (OR = 2.37; 95% CI = 1.57–3.16) and ≥61 years (OR = 5.01; 95% CI = 2.89–7.13), were more likely to become infected with intestinal parasites, compared with the respondents below 40 years of age.
The respondents were also interviewed about their general characteristics and demographic information. Regarding personal health, respondents from both groups exhibited different BMI ranges, but most had a normal BMI. Furthermore, most respondents who were diagnosed with IPI had comorbidities, whereas noninfected respondents mostly denied having comorbidities. Respondents with comorbidities, including gout, hypertension, diabetes, colon cancer, allergy, and cerebral vascular obstruction, were at a much greater risk of IPI than respondents without underlying diseases (OR = 13.23; 95% CI = 6.59–26.55).
Respondents from both groups had relatively low levels of educational attainment. Most had completed primary education programs. Nonetheless, educational level did not contribute to the risk of IPI.
Agriculture-related occupations, including farming and gardening, were the primary occupations of respondents in the infected (68.3%) and noninfected (79.8%) groups. Although agriculture carries a risk of IPI through contact with contaminated environmental reservoirs, in this study, these occupations were not found to be a risk factor for IPI; in fact, they were demonstrated to be significant protective factors against IPI (OR = 0.09; 95% CI = 0.11–0.76).
Economic status was assessed on the basis of monthly income. Most respondents from both groups earned a monthly income of between $30 and $150 per month, with a median income in both groups of $100 per month. The income of the respondents in Khong Chiam was lower than the average monthly income per household in Ubon Ratchathani in 2021, which amounted to ∼$620.80 per month (according to the Annual Report of Provincial Household Income and Income Distribution 2021, Economic Statistics Analysis and Forecasting Group, National Statistical Office, Thailand). Although the respondents had poor economic status, their poor household economy did not influence infection with intestinal parasites.
The respondents were also interviewed about their activities. Respondents from the infected and non-infected groups mainly raised domestic animals (cats and dogs) and livestock (cows and buffalos) near their houses. Although these animals are natural hosts for many parasites, raising them near houses was not a risk factor for IPI (OR = 0.31; 95% CI = 0.17–0.57); in contrast, it appeared to be a protective factor against IPI.
Most respondents from the infected (88.5%) and noninfected (84.6%) groups fed their animals leftover food from their families. Similar behavior of feeding animals leftover food among respondents from both groups made this behavior less likely to promote IPI. Toilets are the basic sanitary infrastructure supplied to all houses, and all respondents regularly defecated in the toilets. Thus, the defecation of respondents appears not to be a factor that influences IPI and the contamination of intestinal parasites in environmental reservoirs.
Most respondents from the infected (68.3%) and noninfected (76.9%) groups demonstrated a lack of attention to examining IPI. Most respondents had never undergone a stool examination, with only 24 participants from both groups having had a previous stool examination and a history of infection with different intestinal helminths, including O. viverrini, hookworms, S. stercoralis, and Taenia spp. Nineteen participants with IPI in this study (18.3%) had a history of previous IPI. A previous positive result for IPI was found to be a significant risk for current IPI (OR = 4.28; 95% CI = 1.51–12.06)
The number of respondents from both groups with a history of taking anthelmintic drugs was higher than the number of respondents with a history of parasitic infection. Thus, the overuse of anthelmintic drugs was indicated among respondents from both groups. Furthermore, the respondents who had a history of taking anthelmintic drugs had a significantly increased risk of infection with intestinal parasites compared with the respondents who had never taken anthelmintic drugs (OR = 4.37; 95% CI = 2.40–7.95; Table 2).
Knowledge regarding IPI.
In the knowledge assessment, respondents from the infected (42.3%) and noninfected (65.4%) groups knew about the risk of infection with O. viverrini from consuming raw freshwater fish. Nonetheless, most respondents from both groups misunderstood and lacked knowledge of the risk of infection with other intestinal helminths from consuming uncooked dishes made from various natural products, such as shrimp, snails, pork, and beef.
Furthermore, the interviews revealed that most respondents from both groups lacked knowledge of intestinal helminth and protozoa transmission routes. Thus, they indicated that they still engaged in several unhygienic behaviors, including passing food into their mouths with dirty hands, consuming unpeeled or unwashed fruits and vegetables, walking barefoot, and consuming food contaminated by flies, that increase the risk of infection with food-borne and soil-transmitted helminths (Supplemental Table 1).
The respondents who had a one-point increase in their score on knowledge about IPI had a 29% lower chance of being infected with intestinal parasites (OR = 0.71; 95% CI = 0.58–0.87; Table 3 and Supplemental Table 1).
Table 3.
Scores for participants’ knowledge and perceptions of intestinal parasitic infection and cholangiocarcinoma, along with their probabilities of being infected with endemic intestinal parasites
| Factors | Average Scores | OR | 95% CI | P-Value | |
|---|---|---|---|---|---|
| Parasite-Infected Respondents (SD) | Non-Parasite-Infected Respondents (SD) | ||||
| Knowledge regarding intestinal parasite infections | 1.23 (1.18) | 1.93 (1.67) | 0.71 | 0.58–0.87 | 0.001 |
| Health perceptions of intestinal parasite infections | 3.17 (1.64) | 4.05 (1.63) | 0.72 | 0.61–0.86 | <0.001 |
| Knowledge regarding cholangiocarcinoma | 1.97 (1.32) | 1.77 (1.43) | 0.92 | 0.77–1.10 | 0.375 |
| Health perceptions of cholangiocarcinoma | 0.55 (0.89) | 0.82 (0.63) | 0.63 | 0.44–0.91 | 0.014 |
| Promoting factors for good hygiene practices | 2.25 (0.94) | 2.93 (0.25) | 0.19 | 0.10–0.37 | <0.001 |
OR = odds ratio.
Health perceptions regarding IPI.
In the questionnaire, eight statements were used to assess the health perceptions of IPI. Respondents from the infected and noninfected groups lacked accurate information on the role of anthelmintic drugs. They perceived anthelmintic drugs to be safe and were more likely to take anthelmintic drugs frequently without concerns about side effects. In addition, respondents from both groups lacked knowledge about the value of fecal examination to confirm IPI before taking anthelmintic drugs.
Respondents from the infected (34.6%) and noninfected (73.1%) groups were aware of O. viverrini infection and the risk of CCA; however, some respondents still perceived opisthorchiasis as harmless. Thus, respondents who perceived anthelmintic drugs as safe and effective were more likely to continue consuming raw freshwater fish.
Respondents from the infected (45.2%) and noninfected (80.8%) groups expressed positive attitudes toward maintaining good health through the consumption of cooked and healthy foods. Furthermore, 57.7% of the infected and 81.7% of the noninfected participants considered the nutritional value of foods, rather than just the taste, as important for personal good health (Supplemental Table 2). Respondents with a one-point increase in health perception scores regarding IPI were 28% more likely to have a significantly reduced risk of IPI (Table 3 and Supplemental Table 2).
Knowledge regarding CCA.
Respondents from the infected (34.6%) and noninfected (23.1%) groups were aware of the risk of re-infection with O. viverrini and CCA. However, all respondents from both groups lacked information on the presence of carcinogens in fermented foods. However, 36.5% of infected and 25% of noninfected participants agreed that consuming fermented foods increased the chance of developing CCA in patients with opisthorchiasis.
In addition, 48.1% of infected and 85.6% of noninfected participants agreed to immediately treat opisthorchiasis to avoid CCA, and 58.7% of infected and 63.5% of noninfected participants agreed to stop consuming uncooked freshwater fish to avoid CCA. However, the scores of the two groups of respondents in this section were not statistically significant in reducing the risk of IPI (Table 3 and Supplemental Table 3).
Health perceptions regarding CCA.
Respondents from the infected and noninfected groups understood that healthy people could be at risk of CCA, which is an avoidable fatal disease (Supplemental Table 4). Although there were respondents who lacked knowledge and had inaccurate perceptions regarding CCA, respondents with a one-point increase in CCA-related health perception scores had a reduced risk of infection with intestinal parasites (OR = 0.63; 95% CI = 0.44–0.91; Table 3).
Factors that promote good hygiene practices.
The interviews revealed that the high cost contributed to most respondents’ unwillingness to undergo CCA treatment. Furthermore, knowledge about O. viverrini infections linked to CCA is essential for encouraging respondents from infected and noninfected groups to discontinue consuming uncooked freshwater fish. In addition, participants’ loved ones and families played a crucial role in encouraging most respondents from both groups to change their unhealthy behaviors and aspire to maintain good health and live longer (Supplemental Table 5). According to the interviews, respondents with a one-point increase in the score related to promoting factors for good hygiene were significantly less likely to be infected with intestinal parasites (OR = 0.19; 95% CI = 0.10–0.37; Table 3).
DISCUSSION
This survey is the first report to reveal the prevalence of intestinal helminth and protozoan infections in participants in the rural area of Khong Chiam. The predominance of strongyloidiasis and the high prevalence of opisthorchiasis and other intestinal parasites in Khong Chiam imply that these infections are currently endemic, owing to the number of food-borne and soil-transmitted parasites, as well as the presence of unhygienic behavior among participants.
The prevalence of IPI in Khong Chiam was higher in males than females, which aligns with the findings many previous reports in the northeast.1–4 Susceptibility to infection and male-specific unsanitary behaviors may promote more frequent infections in males than females.15,16 Opisthorchiasis, however, was equally prevalent in both sexes, indicating that raw freshwater fish consumption behavior is shared between both sexes. In addition, the report of opisthorchiasis in a young boy from this survey suggests that sharing undercooked food in the family contributes to the prevalence of O. viverrini infections.17
Age, comorbidities, history of parasitic infections, and history of taking anthelmintic drugs were related to the IPI status of the participants in Khong Chiam. Older adults were more likely to be infected with intestinal parasites than younger adults. Long-term and frequent exposure to parasite infection stages and the aging immune system of older adults may increase susceptibility to parasitic infections.18 Furthermore, IPI in older patients, particularly strongyloidiasis, should be given attention because there is a chance of autoinfection, resulting in persistent hyperinfection syndrome and disseminated disease.19
Comorbidities, which are long-lasting chronic diseases such as metabolic syndrome, allergy, and cancer, can cause gradual dysfunction and malfunction in the body. Thus, participants with comorbidities are susceptible to IPI and may develop severe infections.20 Furthermore, abnormal BMI levels can impair immune function and promote susceptibility to infection.21 Thus, monitoring IPI in participants with abnormal weights should be considered.
The lack of knowledge and inaccurate perceptions regarding various aspects of IPI and CCA were observed among participants in Khong Chiam. Inaccurate perceptions regarding the safety and efficiency of anthelminthic drugs can cause participants to pay less attention to modifying their unsanitary behaviors and having samples tested for parasitic infections. Thus, they can be at risk of reinfection with several endemic parasites. This is consistent with findings of the interviews, which revealed that participants who had previously experienced parasitic infection were more likely to be at risk of IPI. The availability of inexpensive anthelmintic drugs in drug stores can also promote self-treatment and the frequent and excessive use of anthelmintic drugs, leading to drug overdoses and side effects that may interfere with daily work and life.4 Furthermore, the overuse of anthelmintics, the repeated use of the same class of anthelmintics, and the use of anthelmintics at suboptimal doses contribute to increased anthelmintic drug resistance.22 Additionally, the interview revealed that the inappropriate use of anthelmintic drugs can promote the risk of IPI. Thus, rational anthelmintic drug use must be oriented toward appropriate dose and duration, clinical need, and enhancing patients’ knowledge of side effects to promote effective, safe, and economical dispensing.
This study revealed that primary occupations aligned with agriculture and low income were not risk factors for infection with endemic intestinal parasites. However, agricultural occupations can cause participants to come into contact with contaminated soil and freshwater reservoirs. Furthermore, the poor economic status of the participants may have prevented them from purchasing necessities to prevent IPI and engaging in traditional farming. Thus, the provision of protective equipment and the promotion of modern agriculture should be considered.23
Furthermore, several activities, such as raising animals near houses and feeding animals leftover food, were common in Khong Chiam and were not risk factors for IPI in participants. However, these activities can spread the parasite infective stage and allow for IPI in animals, as well as participants.
Furthermore, this survey revealed that the participants in Khong Chiam knew about the association between opisthorchiasis and CCA, but they lacked knowledge on the occurrence and risk of CCA. They also still perceived CCA as an unavoidable disease, which may have reduced their motivation to change their behavior and seek treatment. However, the participants, as well as their loved ones and families, wished to live long and healthy lives. Additionally, the high cost of medical treatment motivated participants to modify their behaviors and engage in better hygiene habits to avoid IPI and CCA.
Therefore, an array of conventional approaches involving collaboration between public health agencies and communities to provide knowledge that motivates behavior modification, provide anthelmintic drug treatment, and improve basic environmental and sanitary conditions remains essential in the villages of Khong Chiam. Nonetheless, a subtle emphasis on the importance of sanitary practices and reminding villagers of hygienic behaviors are essential for achieving sustainable outcomes and cost-effectiveness. Furthermore, fostering open and supportive communication within a family is necessary in Khong Chiam because family and loved ones impact participants’ behavioral changes. Individuals who communicate with their families may feel more supported and empowered to make healthy decisions.24
Supplemental Materials
ACKNOWLEDGMENTS
We would like to thank the public health officers and village health volunteers of health-promoting hospitals for facilitating the research and sample collection in Khong Chiam District, all project participants for their attendance and for being the key to the project’s success, the technicians at the laboratory of the College of Medicine and Public Health, Ubon Ratchathani University, for offering the resources to perform the work, and Editage (www.editage.com) for English language editing.
Note: Supplemental materials appear at www.ajtmh.org.
Data Availability
All relevant data are available in the manuscript and supporting information files.
REFERENCES
- 1.Sangwalee W. et al. , 2022. Prevalence of intestinal parasitic infections and genetic differentiation of Strongyloides stercoralis among migrant workers from Myanmar, Lao PDR and Cambodia in northeastern Thailand. PLoS One 17: e0279754. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Laoraksawong P, Sanpool O, Rodpai R, Thanchomnang T, Kanarkard W, Maleewong W, Kraiklang R, Intapan PM, 2018. Current high prevalences of Strongyloides stercoralis and Opisthorchis viverrini infections in rural communities in northeast Thailand and associated risk factors. BMC Public Health 18: 940. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Chaiputcha K, Promthet S, Bradshaw P, 2015. Prevalence and risk factors for infection by Opisthorchis viverrini in an urban area of Mahasarakham Province, Northeast Thailand. Asian Pac J Cancer Prev 16: 4173–4176. [DOI] [PubMed] [Google Scholar]
- 4.Boonjaraspinyo S. et al. , 2022. Prevalence and associated risk factors of intestinal parasitic infections: A population-based study in Phra Lap Sub-District, Mueang Khon Kaen District, Khon Kaen Province, Northeastern Thailand. Trop Med Infect Dis 8: 22. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Chuangchaiya S, Laoprom N, Idris ZM, 2019. Prevalence and associated risk factors of Opisthorchis viverrini infections in rural communities along the Nam Kam River of Northeastern Thailand. Trop Biomed 36: 81–93. [PubMed] [Google Scholar]
- 6.Anamnart W, Intapan PM, Maleewong W, 2013. Modified formalin-ether concentration technique for diagnosis of human strongyloidiasis. Korean J Parasitol 51: 743–745. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Viravan C, Bunnag D, Harinasuta T, Upatham S, Kurathong S, Viyanant V, 1986. Clinical field trial of praziquantel in opisthorchiasis in Nong Rangya Village, Khon Kaen Province, Thailand. Southeast Asian J Trop Med Public Health 17: 63–66. [PubMed] [Google Scholar]
- 8.Bunnag D, Harinasuta T, 1980. Studies on the chemotherapy of human opisthorchiasis in Thailand: I. clinical trial of praziquantel. Southeast Asian J Trop Med Public Health 11: 528–531. [PubMed] [Google Scholar]
- 9.Rim HJ, Park SB, Lee JS, Joo KH, 1979. Therapeutic effects of Praziquantel (Embay 8440) against Taenia solium infection. Kisaengchunghak Chapchi 17: 67–72. [DOI] [PubMed] [Google Scholar]
- 10.Chai J, Sohn W, Hong S, Lee S, Seo B, 1985. Anthelmintic effect of praziquantel (Cestocide@) in the treatment of Taenia saginata and Diphyllobothrium latum infection. J Korean Soc Chemother 3: 181–184. [Google Scholar]
- 11.Viravan C, Migasena S, Bunnag D, Harinasuta T, 1982. Clinical trial of albendazole in hookworm infection. Southeast Asian J Trop Med Public Health 13: 654–657. [PubMed] [Google Scholar]
- 12.Charoenlarp P, Bunnag D, 1986. Treatment of parasitic infections in Thailand. Southeast Asian J Trop Med Public Health 17: 620–626. [PubMed] [Google Scholar]
- 13.Gardner TB, Hill DR, 2001. Treatment of giardiasis. Clin Microbiol Rev 14: 114–128. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Laymanivong S, Hangvanthong B, Keokhamphavanh B, Phommasansak M, Phinmaland B, Sanpool O, Maleewong W, Intapan PM, 2014. Current status of human hookworm infections, ascariasis, trichuriasis, schistosomiasis mekongi and other trematodiases in Lao People’s Democratic Republic. Am J Trop Med Hyg 90: 667–669. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Zuk M, McKean KA, 1996. Sex differences in parasite infections: Patterns and processes. Int J Parasitol 26: 1009–1023. [PubMed] [Google Scholar]
- 16.Bertoncello C, Amoruso I, Moscardino U, Fonzo M, Maharjan M, Buja A, Baldo V, Cocchio S, Baldovin T, 2021. Sex-biased prevalence of intestinal parasitic infections and gender inequality in rural Nepal. Int J Infect Dis 109: 148–154. [DOI] [PubMed] [Google Scholar]
- 17.Phimpraphai W, Tangkawattana S, Kasemsuwan S, Sripa B, 2018. Social influence in liver fluke transmission: Application of social network analysis of food sharing in Thai Isaan culture. Adv Parasitol 101: 97–124. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Albright JW, Albright JF, 1994. Ageing alters the competence of the immune system to control parasitic infection. Immunol Lett 40: 279–285. [DOI] [PubMed] [Google Scholar]
- 19.Lamptey AN. et al. , 2023. Regular Deworming and Seasonality Are Potential Challenges but Also Offer Opportunities for Hookworm Elimination. Available at: https://www.medrxiv.org/content/10.1101/2023.03.09.23287064v1. Accessed December 10, 2024.
- 20.Rennie C, Fernandez R, Donnelly S, McGrath KC, 2021. The impact of helminth infection on the incidence of metabolic syndrome: A systematic review and meta-analysis. Front Endocrinol (Lausanne) 12: 728396. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Ray A, Bonorden MJL, Pandit R, Nkhata KJ, Bishayee A, 2023. Infections and immunity: Associations with obesity and related metabolic disorders. J Pathol Transl Med 57: 28–42. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Shalaby HA, 2013. Anthelmintics resistance; how to overcome it? Iran J Parasitol 8: 18–32. [PMC free article] [PubMed] [Google Scholar]
- 23.Paller VGV, Macalinao-Ramirez CA, Bandal MZ, 2022. Environmental contamination with parasites in selected rural farms in the Philippines: Impacts of farming practices on leafy greens food safety. Parasitology 149: 482–489. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Rosland AM, Heisler M, Piette JD, 2012. The impact of family behaviors and communication patterns on chronic illness outcomes: A systematic review. J Behav Med 35: 221–239. [DOI] [PMC free article] [PubMed] [Google Scholar]
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Supplementary Materials
Data Availability Statement
All relevant data are available in the manuscript and supporting information files.