Infection Status of Endoparasites in Foreigner Workers Living in Cheonan City, Chungnam Province, Korea

In 2013, the number of foreigners working as factory laborers in Korea was approximately 500,000 [1]. Chinese was the most common nationality, accounting for almost a half (47.1%) of the total worker pool, followed by Vietnamese (12.1%), Indonesian (5.3%), Uzbekistani (4.6%), Thailander (4.1%), and Filipino (3.9%), among others [1]. These nations are still known as endemic areas of parasitic infections, for example, according to a recent survey conducted in Vietnam, 47% of the study population was positive for parasites such as Ascaris lumbricoides (24%), Trichuris trichiura (40%), and Entamoeba histolytica (6%) [2]. The prospective foreigner workers undergo a pre-employment medical examination; however, no screening test for parasitic infections is included. Most parasitic diseases are easily treatable after early diagnosis, but can cause severe complications if undetected and untreated, thereby negatively impact upon worker’s productivity. Recently in Korea, a 25-year-old Uzbek male complaining of abdominal pain was admitted to a hospital, and finally was diagnosed as cystic echinococcosis [3]. Since he had already been working for 3 years in his home country, early diagnosis through preemployment medical examination certainly would have proved helpful for him and his industry, not to mention Korea. In advanced countries, unsurprisingly, screening of foreigner workers for parasitic infections is frequently carried out. In Japan, a dot-ELISA showed 28.4% to be positive for parasites, toxoplasmosis being the most common [4]. In Taiwan, a stool survey identified 7.4% of workers as positive, among whom the most common nationality was Vietnamese [5]. In Italy, the parasitic infection prevalence among immigrants between 2008 and 2009 was 61.9% [6]. However, no investigations of parasitic infection prevalence among foreigner workers have yet been conducted in Korea. The present study was conducted to determine the parasitic infections of foreigner workers living in Cheonan-si (City), Chungcheongnam-do (Province) and at the same time to lay the initial groundwork for future infection-control measures.

With the help of the Cheonan Support Center for Foreigner Workers, small businesses employing foreigner workers in Cheonan-si were selected from October to December, 2013. A total of 231 foreigner workers, 218 males and 13 females, provided samples. Among the 11 nationalities represented, the most common was Nepalese (33.8%), followed by Chinese, Indonesian, Uzbekistani, Vietnamese, and the rest. The study subjects ranged in age from 20s to 50s, most of them being in their 20s (42.0%) and 30s (36.4%). After informing the workers of the significance and necessity of this research, they were asked to provide a single fecal sample and to bring it at their workplace on the scheduled day. On that same day, blood sampling was performed and relevant personal information was obtained. The fecal samples were transferred to a laboratory where they were subjected to processing by both the KatoKatz thick smear technique and formalin-ether concentration technique preparatory to microscopic examinations.

Each blood sample was centrifuged and stored refrigerated in the laboratory prior to ELISA testing for parasitic infections. ELISA was performed in the laboratory of the Institute of Endemic Diseases, Seoul National University College of Medicine, targeting Clonorchis sinensis, Paragonimus westermani, metacestode of Taenia solium (Cysticercus cellulosae), sparganum, Toxocara canis, and Echinococcus granulosus. The employed antigens of these helminths included crude extracts of C. sinensis and P. westermani, cystic fluid of T. solium metacestode, crude saline extract of spargana, and excretory-secretory antigen of Toxocara canis larvae. The utilized sera, both negative and positive controls were collected, respectively, from healthy students and single-antibody-positive patients who had been diagnosed previously by routine ELISA. The positive criteria of ELISA absorbance were 0.250 in clonorchiasis, 0.280 in paragonimiasis, 0.290 in cysticercosis, 0.240 in sparganosis, 0.250 in toxocariasis, and 0.270 in echinococcosis, all of which were calculated from raw empirical data.

As indicated in Table 1, a total of 60 foreigner workers from 11 countries were found to be infected with parasites; the overall infection rate was 26.0% (60/231). The stool examination detected 14 positive cases (6.1%), 2 of which showed concurrent infections with 2 kinds of parasites. Hookworms and Trichostrongylus orientalis eggs were observed in 3 cases each, and those of C. sinensis and T. trichiura in 2 cases each (Table 1). Protozoan cysts were also detected, those of Giardia lamblia, found in 3 workers, being the most common species. Cysts of Entamoeba coli, Endolimax nana, and Entamoeba histolytica or E. dispar were discovered as well (Table 1). Most of the positive cases were detected by serological examinations. In ELISA, 50 (21.6%) of the 231 workers were positive for at least 1 kind of parasitic disease. The most common infection was cysticercosis (8.7%), followed by toxocariasis (7.8%), clonorchiasis (7.4%), and echinococcosis (3.5%). Paragonimiasis was detected only in 2 workers (Table 1). Among the 11 nationalities represented in this study, the highest numbers of positive cases were detected in Nepalese (20), Chinese (9), and Indonesian (8) workers, though the highest infection rate was found among Sri Lankan workers (44.4%) (Table 2). All the workers tested positive by stool examinations were provided the anthelmintic drugs such as albendazole (400 mg, once) and praziquantel (40 mg/kg, once). Those showing protozoa or serum antibody positive cases, meanwhile, were directed to health screening centers where they could be treated for parasites.

Table 1.

Positive rate of parasites in fecal and serological examinations by their countries

Table 2.

Number of positive workers for each helminth or protozoa detected either by stool examination or ELISA

The summary judgment of this study was that parasitic infections were prevalent among foreigner workers living in Cheonan-si, Chungcheongnam-do. The overall infection rate, based on both serological and stool examinations, was 26.0%, much higher than that reported for the general Korean population, 2.6%, in 2012 [7]. Although this Korean rate had been calculated by stool examination only, it is still less than half of the present study’s stool positivity rate, 6.1%. This was similar to the stool positivity of foreigner workers in Taiwan, 7.4% [5]. As for the serum antibody positive rate in the present study, 21.6%, it was slightly lower than that of the foreigner workers in Japan, 28.4% [4,5]. Particularly, given that most parasitic diseases are easily treated with anthelmintic drugs, screening for parasitic infections among foreigner workers is needed in order to ensure early diagnosis and treatment.

The prevalence rate of C. sinensis in our study was 7.4%. However, eggs were recovered from only 1 stool sample of an Uzbekistani, where C. sinensis is not distributed [8]. Except for Chinese and Vietnamese, the seropositive cases were those from non-endemic areas of clonorchiasis [8]. In this regard, they might be infected with C. sinensis after their immigration to Korea. Another possible explanation is related to the present study’s use of a crude extract antigen in ELISA test, which reduced the sensitivity and specificity to 88.2% and 87.8%, respectively [9]. Considering that the serum of the stool positive patients was not reacted to C. sinensis antigen in this study, it was speculated that there could be more false negativities in this population.

Protozoan cysts such as G. lamblia, E. coli, E. nana, and another Entamoeba sp., were discovered in the present study. Although E. coli and E. nana have been known to be non-pathogenic, the foreigner workers infected with Entamoeba sp. and G. lamblia were symptom-free. This phenomenon might be better understood in light of the fact that giardiasis is symptomatic only about 50%, and that the Entamoeba sp. in the present case may be E. dispar, the known gut commensal [10,11].

The most common parasitic infection encountered in this study was cysticercosis (8.7%), and nearly a half (40%) of the cases was among Nepalese workers. According to a previous report from Nepal, the positive rate for T. solium ranged from 10% to 50% in some districts, and for porcine cysticercosis, 32.5% [12]. In the present study, seropositive cases for cysticercosis were also found in workers from Sri Lanka, Kazakhstan, Indonesia, China, and Vietnam, and in the latter 3 countries, the presence of cysticercosis was confirmed [12]. It was also noteworthy that 8 workers (3.5%), mostly Napalese (5 individuals), tested serologically positive for hydatid disease. Even though indigenous cases have been reported in Korea, it is probable that the foreigner workers tested in the present study had been infected with hydatid disease in their homelands [13]. In fact, Nepal is an endemic country for hydatid disease which involves the breast [14]. Further work-up on these patients is urgently required, especially in consideration of the fact that hydatid disease can lead to medical emergencies such as in the case of an Uzbek worker [3] noted earlier in this paper.

Notwithstanding the sharply decreasing tendencies in the Korean rates of parasitic infections, rates remain high in some other Asian countries. Laborers of those nationalities working in Korea might suffer from parasitoses during their stay, or, still more seriously, could unwittingly facilitate the comeback of parasites that had already been eradicated from Korea. Therefore, their infection status should be checked carefully, not only to protect those workers in the short term but also to establish and build the kinds of database that will be essential to any future Korean parasite-control programs. The present study can be considered to be inaugural in both respects, but has a limitation that the foreigner workers only in Cheonan-si were selected for parasitological examinations. At present, a large number of foreigner workers have been working in various areas such as Gyonggi-do, Seoul, Gyongsangnam-do, and Inchon. Hence, more comprehensive study on those areas is urgently needed in order to understand the parasitic infections of foreigner workers in Korea.