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Active screening of gastrointestinal helminth infection in migrant workers in Thailand

Objective This study aimed to detect gastrointestinal helminth infection in migrant workers in Thailand. Methods A cross-sectional survey study was conducted in 403 migrant workers in the factories of Nakhon Ratchasima Province, northeastern Thailand during October 2016 to June 2017. Gastrointestinal helminth infections were detected by the formalin ether acetate concentration technique and microscopy. The data were analyzed using the χ2-test and logistic regression. Results The rate of gastrointestinal helminth infection was 24.07%. The most common species involved in infection was Opisthorchis viverrini (11.91%), followed by hookworm (5.46%), Trichuris trichiura (5.21%), Strongyloides stercoralis (0.5%), Ascaris lumbricoides (0.5%), and Taenia spp. (0.5%). The majority of infections were found in men aged ≥40 years, married participants, uneducated participants, laborers, those who worked for 1 year, and those who had an income of 9000 to 12,000 THB. Conclusions Gastrointestinal helminth infection is still found in migrant workers. Therefore, active surveillance is required in this large group for investigating and eradicating this type of infection.


Introduction
Gastrointestinal helminth infections remain a serious health problem worldwide, including in Southeast Asian nations (ASEAN), particularly in Lao People's Democratic Republic (PDR), Cambodia, and Myanmar. The most common gastrointestinal helminth infections are neglected tropical diseases that are associated with approximately 300 million infections in these regions. Among soil-transmitted helminth (STH) infections, 126.7 million people in ASEAN are infected with Ascaris lumbricoides, 115.3 million are infected with Trichuris trichiura, and 77.0 million have hookworm infections. Additionally, more than 10 million people suffer from either liver or intestinal fluke infections. 1 Liver fluke, including Opisthorchis viverrini and Clonorchis sinensis, are classified as Group 1 carcinogens by the World Health Organization's International Agency for Research on Cancer. 2 O. viverrini infection is associated with cholangitis, gallstones, hepatomegaly, cholecystitis, and cholangiocarcinoma. [3][4][5][6][7][8] Infection by these gastrointestinal helminth infections is rarely diagnosed at early exposure and is thus frequently asymptomatic. Persistent and chronic infection can cause severe cancer complications, particularly cholangiocarcinoma and other gastrointestinal diseases. 9 Gastrointestinal helminth infection in ASEAN has spread because of increased labor migration among ASEAN Economic Community countries (Lao PDR, Thailand, Myanmar, Vietnam, and Cambodia) as a result of an open borders policy that was started in 2015. 10 Therefore, gastrointestinal helminth infection constitutes an important and serious health problem in ASEAN and eradication of the infection is urgently required in these areas. A pilot project was conducted in migrant workers in factories from Nakhon Ratchasima Province, northeastern Thailand. This study aimed to detect gastrointestinal helminth infections, which included intestinal tapeworms, roundworms, and liver flukes, in migrant workers. We used the formalin ethyl acetate concentration method to detect gastrointestinal helminth infections and then treated the infections and provided health education.

Ethical considerations
This study was approved by the Ethics Committee for Research Involving Human Subjects of Suranaree University of Technology, Thailand (EC-59-39). Before participating in the study, all participants provided written informed consent. Permission was granted by the owners of the factories.

Study areas
A cross-sectional survey pilot study was performed in migrant workers in the Nakhon Ratchasima area, which is in the northeast region of Thailand. Nakhon Ratchasima (often called Khorat) is one of the northeast provinces of Thailand. This area is the country's largest province by area (20,494 square kilometers [7,913 square miles]), with a population of approximately 2.7 million (the country's second largest province in terms of the number of people). Nakhon Ratchasima produces approximately 250 billion THB in GDP, which is the highest in the northeast region. Nakhon Ratchasima is 259 kilometers (161 miles) from Bangkok, which is the capital of Thailand. This province is divided into 32 districts, 263 sub-districts, and 3743 villages (Department of Provincial Affairs, 2015).

Study population
There are currently 1,778,964 migrant workers in Thailand. The majority of these workers (approximately 1,563,269 workers) are from Myanmar, Cambodia, and Lao PDR. There were 8,146 migrant workers in Nakhon Ratchasima Province during October 2016 to June 2017. These workers included 4267 in Myanmar, 2670 in Cambodia, and 1209 in Lao PDR (foreigner workers administration office, Thailand, 2017). Participants included 193 among 8,146 who worked in Sung Neon, Khon Buri, and Pak Chong District, Nakhon Ratchasima Province. We further included one fold the amount of participants for the best representative population (n ¼ 386 participants). A further 17 migrant workers were interested in participating in this screening project. Therefore, we asked permission from their employers and then included the workers in the study. Consequently, the total population of this study was 403 migrant workers. Purposive sampling of the participants was according to those who were interested and the factories' permission.

Survey
We used a constructive questionnaire, which included important questions on sociodemographic characteristics and the working period in Thailand. A questionnaire survey was conducted among the participants while we collected their stool samples. All questionnaires were translated to languages used in Myanmar, Cambodia, and Lao PDR. Participants completed the questionnaires by themselves.

Stool sample collection and examination
Stool specimens of all participants were collected in plastic containers (protected transmission) and then transferred to the standard laboratory of the Parasitic Disease Research Center at Suranaree University of Technology. The presence of gastrointestinal helminth eggs, including flukes, tapeworms, and roundworms, was determined by using the formalin ether concentration method. 11 Briefly, 1 g of each fecal sample was selected and then fixed with 10% formalin in a 10-mL test tube. The specimen was further processed according to the formalin ethyl acetate method and then examined for gastrointestinal helminth infections. Each specimen was examined under a microscope, and initially screened with a low-power objective lens. Suspected gastrointestinal helminths were subsequently examined under a high-power objective lens with a microscope. All of the samples were examined by two laboratory technologists from the Parasitic Disease Research Center. Patients who were infected with gastrointestinal helminths and other known parasites were treated with antigastrointestinal helminth drugs and also asked to attend health education.

Data analysis
Statistical analyses were performed using SPSS Version 22.0 (IBM Corp., Armonk, NY, USA). The v 2 test was used for computing differences in infections and characteristics. A P value of < 0.05 was considered statistically significant. Unconditional logistic regression was used to analyze the positive rate of eggs and their characteristics.
The majority of gastrointestinal helminth infections were found in men (25.0%), those aged 40 years old (27.0%), those who were uneducated (30.3%), those who were married (23.2%), laborers (21.6%), those who worked for 1 year (37.8%, P < 0.001 vs 2-3 yearsþ, v 2 test), those who had an income of 9000 to 12,000 THB (22.8%), those who worked at factory sites in Pak Chong District (28.6%, P ¼ 0.003 vs Sung Neon and Khon Buri Districts, v 2 test), and those who stayed in private dormitories (25.0%) ( Table 2). By nationality, the positive rate of gastrointestinal helminth eggs that were detected in workers from Cambodia was 27.27%, followed by 22.87% in Myanmar, and 22.03% in Lao PDR. Linear regression analysis showed that nationality, sex, age, education, marital status, occupation, and income (THB) were not significantly associated with gastrointestinal helminth infections (Table 3).

Discussion
Poverty and neglected tropical diseases are found in ASEAN. 1 Pullan et al. 12 reported that 126.7, 115.3, and 77.0 million people are infected with A. lumbricoides, T. trichiura, and hookworm, respectively. An infection with STH can lead to malnutrition in children and older aged people. STH infections may impair cognitive development and growth in children. The present study examined the overall infection rate  [13][14][15] O. viverrini is commonly found in Lao PDR, particularly in the central and southern areas, and it constitutes a serious health problem. Vonghachack et al. 13 showed that the infection rate and heavy intensity  17 Their stool surveys of rural populations in three regions showed that the positive rate of Opisthorchis eggs was 9.30%. Our study is the second report of O. viverrini infection in humans from Myanmar, but is the first report on people from Myanmar who migrate to work in Thailand.
Other gastrointestinal helminth eggs were detected in migrant workers in our study, particularly hookworm (5.46%), T. trichiura (5.21%), S. Stercoralis (0.50%), A. lumbricoides (0.50%), and Taenia spp. (0.50%). The positive rate of gastrointestinal helminth eggs that were detected was highest in migrant workers from Cambodia, followed by Myanmar and Lao PDR. Gastrointestinal helminth infections in migrant workers included Our study showed that characteristics such as nationality, sex, age, education, marital status, occupation, and income were not associated with gastrointestinal helminth infections. Therefore, our demographic data could not explain gastrointestinal helminth infections. The prevalence of parasitic species of O. viverrini, hookworm, and T. trichiura in Southern Lao PDR has been previously reported. 13 O. viverrini infection appears to be acquired at a young age, and its prevalence gradually increases with age. Hookworm infection is also acquired at a young age. The prevalence of hookworm peaks in adolescents aged 10 to 20 years and plateaus in older age groups in men and women. The prevalence of T. trichiura is distributed similarly among men and women independent of age. 13 The associations of risk factors with S. stercoralis were studied in Myanmar and its prevalence did not significantly differ between men and women (P ¼ 0.193). However, the prevalence of S. stercoralis infection significantly increased with age (P ¼ 0.041). 21 Occupation and income in our study were not associated with gastrointestinal helminth infections.
Many studies have shown that gastrointestinal helminth infections are neglected tropical diseases and they are recognized as a major public health concern in many low-and middle-income countries in the tropics and sub-tropics, including in Myanmar, Cambodia, and Lao PDR. [22][23][24][25] STHs are among the most prevalent infections in these three countries. Liver fluke, O. viverrini, and Taenia spp. are endemic in Thailand, Cambodia, and Lao PDR. Infections with these helminths negatively affect human health and wellbeing. The high gastrointestinal helminth infection rate in this study and previous studies in migrant workers is a serious public health problem. The effect of gastrointestinal