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 O pisthorchis 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.[3-8] 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.

Materials and methods

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 = 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 anti-gastrointestinal 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 χ2 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.

Results

Among the 403 participants surveyed, 97 (24.07%) were positive for gastrointestinal helminth infections. The highest rate of infection was due to O. viverrini (11.91%), followed by hookworm (5.46%), T. trichiura (5.21%), S. Stercoralis (0.50%), A. lumbricoides (0.50%), and Taenia spp. (0.50%). Gastrointestinal helminth eggs were found in fecal samples from the 403 participants (Table 1).

Table 1.

Gastrointestinal helminth infection in 403 migrant workers in Nakhon Ratchasima Province, Northeastern Thailand.

Nationality	No. of participants	No. of infections (%)		Intestinal helminth infection
				(no. of infections (%))
			Opisthorchis viverrini	Hookworm	Trichuris trichiura	Strongyloides stercoralis	Ascaris lumbricoides	Taenia spp.
Myanmar	223	51 (22.87)	8 (3.43)	19 (8.15)	21 (9.01)	1 (0.45)	2 (0.90)	0 (0)
Cambodia	121	33 (27.27)	31 (25.62)	1 (0.83)	0 (0)	1 (0.83)	0 (0)	0 (0)
Lao PDR	59	13 (22.03)	9 (15.25)	2 (3.39)	0 (0)	0 (0)	0 (0)	2 (3.39)
Total	403	97 (24.07)	48 (11.91)	22 (5.46)	21 (5.21)	2 (0.50)	2 (0.50)	2 (0.50)

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 years+, χ2 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 = 0.003 vs Sung Neon and Khon Buri Districts, χ2 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).

Table 2.

Positive rate of gastrointestinal helminth eggs categorized by general characteristics.

Characteristics	Total	Helminth-negative, n (%)	Helminth-positive, n (%)	χ2 test	P value
Nationality				2.444	0.299
Myanmar	233	182 (78.11)	51 (22.87)
Cambodia	121	88 (72.72)	33 (27.27)
Lao PDR	59	46 (77.97)	13 (22.03)
Sex				1.12	0.29
Female	287	229 (79.80)	58 (20.20)
Male	116	87 (75.00)	29 (25.00)
Age				1.284	0.257
<40 years old	340	270 (79.40)	70 (20.60)
≥40 years old	63	46 (73.00)	17 (27.00)
Education				3.995	0.262
Primary school	274	219 (79.90)	55 (20.10)
Junior secondary school	42	35 (83.30)	7 (16.70)
Senior secondary school	21	16 (76.20)	5 (23.80)
Uneducated	66	46 (69.70)	20 (30.30)
Marital status				2.145	0.143
Single	88	74 (84.10)	14 (15.90)
Married	315	242 (76.80)	73 (23.20)
Occupation				0.015	1
Housekeeper	10	8 (80.00)	2 (20.00)
Laborer	393	308 (78.40)	85 (21.60)
Working period in Thailand				26.309	0.001
1 year	119	74 (62.20)	45 (37.80)
2–3 years	114	122 (84.70)	22 (15.30)
>3 years	140	120 (85.70)	20 (14.30)
Income (THB)				0.793	0.373
<9000	127	103 (81.10)	24 (18.90)
9000–12,000	276	213 (77.20)	63 (22.80)
Factory site (district)				11.403	0.003
Pak Chong District	147	105 (71.40)	42 (28.60)
Sung Neon	223	179 (80.30)	44 (19.70)
Khon Buri	33	32 (97.00)	1 (3.00)
Residency				0.085	0.727
Private dormitory	12	9 (75.00)	3 (25.00)
Factory accommodation	391	307 (78.50)	84 (21.50)

Table 3.

Factors associated with gastrointestinal helminth infection using logistic regression analysis.

Characteristics	OR	95% confidence interval	P value	ORadj	95% confidence interval	P value
Nationality			0.153			0.338
Myanmar	1			1
Cambodia	1.46	0.87–2.46		2.08	0.72–5.98
Lao PDR	0.93	0.45–1.94		1.69	0.58–4.96
Sex			0.291			0.687
Female	1			1
Male	1.32	0.79–2.19		1.19	0.59–2.20
Age			0.259			0.866
<40 years old	1			1
≥40 years old	1.42	0.77–2.64		1.04	0.53–2.11
Education			0.567			0.053
Primary/secondary school	1			1
Uneducated	1.2	0.64–2.23		1.77	0.99–3.59
Marital status			0.146			0.074
Single	1			1
Married	1.59	0.85–2.99		1.84	0.94–3.74
Occupation			0.902			0.791
Housekeeper	1			1
Laborer	1.1	0.23–5.30		1.16	0.20–8.42
Income (THB)			0.374			0.587
<9000	1			1
9000–12,000	0.79	0.47–1.33			0.43–1.60

OR: odds ratio; ORadj: adjusted odds ratio.

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 among migrant workers in Nakhon Ratchasima Province, Thailand and showed that 24.07% of them were positive for gastrointestinal helminth infections.

The highest rate of infection in our study was O. viverrini (11.91%) in the participants. The majority of O. viverrini infections were detected in workers from Cambodia, followed by Lao PDR and Myanmar. Opisthorchiasis has been reported in Cambodia and Lao PDR.[13-15] 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 infection rate of O. viverrini were 60.7% and 4.2%, respectively. Nakamura[14] reported the present situation of helminthic infections in the capital city, Vientiane, and found that the infection rate was high (54%–59%). In particular, O. viverrini infection had the highest rate, ranging from 51% to 53%. Additionally, a field survey in Cambodia with 16,082 stool samples from five provinces showed that 1232 were positive for eggs with O. viverrini infection (7.70%). The endemic areas of O. viverrini infection include four Cambodian provinces.[15] Moreover, the O. viverrini infection rate was 4.6% among 2101 residents along the Mekong River, Kratie Province, Cambodia.[16] In Myanmar, O. viverrini infection was first reported in communities from lower Myanmar by Aung et al.[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 STHs. Also called geohelminths, STHs are a group of intestinal parasites that belonging to the phylum Nematoda and are transmitted primarily through contaminated soil. STHs are typically from the following families of nematodes: A. lumbricoides, T. trichiura, hookworms, and S. stercoralis. In our study, the infection rate of STHs was 45.50% (47 cases among 403 participants; hookworms, 22 cases; T. trichiura, 21 cases; A. lumbricoides, 2 cases; and S. stercoralis, 2 cases), and migrant workers were infected by one or more helminth (Table 1). The rates of STHs, including hookworm, T. trichiura, and A. lumbricoides were higher in Myanmar than in Cambodia and Lao PDR. Additionally, a food-borne helminth infection (Taenia spp.) was found in migrant workers. Our findings indicate that STH and food-borne helminth infections remain a serious problem and may occur in migrant workers. These infections may further spread to other countries during workers’ migration. Sagnuankiat et al.[18] examined gastrointestinal helminth infections in 372 migrant children in Samut Sakhon Province, central Thailand. They found that gastrointestinal helminth infections were highly prevalent, with a rate of 71.0%. These infections were identified as T. trichiura (50.8%), Enterobius vermicularis (25.2%), A. lumbricoides (15.3%), hookworm (11.6%), and Blastocystis hominis (0.5%). Ngrenngarmlert et al.[19] investigated gastrointestinal helminth infections in 213 Myanmar migrant workers in Samut Sakhon and Bangkok Provinces, Thailand. The overall prevalence of gastrointestinal helminth infections was 13.6%, including A. lumbricoides (3.3%) and T. trichiura (2.3%). Nuchprayoon et al.[20] performed a study of gastrointestinal helminth infections in 284 Myanmar migrants who worked in the Thai food industry in Samut Sakhon Province, Thailand. They found that the gastrointestinal helminth infection rate was 62.3%, and identified T. trichiura (22.2%) and A. lumbricoides (1.8%).

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 = 0.193). However, the prevalence of S. stercoralis infection significantly increased with age (P = 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.[22-25] 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 helminth infections on public health is well known. These infections can spread and be transmitted from infected areas to uninfected areas via fecal oral transmission from unclean contaminated water, vegetables, and food.

Conclusions

In conclusion, gastrointestinal helminth infection is common in many migrant workers. To consolidate progress and ascertain long-term sustainability, other control measures, such as active screening on a large scale, treatment, and health education, should be considered for gastrointestinal helminth infection.