Acta Tropica 136 (2014) 74–80

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Prevalence of Haplorchis taichui among humans and fish in Luang Prabang Province, Lao PDR Woon-Mok Sohn a , Tai-Soon Yong b , Keeseon S. Eom c , Duk-Young Min d , Dongmin Lee c , Bong-Kwang Jung e , Virasack Banouvong f , Bounnaloth Insisiengmay g , Bounlay Phommasack g , Han-Jong Rim h , Jong-Yil Chai e,∗ a

Department of Parasitology and Institute of Health Sciences, Gyeongsang National University School of Medicine, Jinju, Republic of Korea Department of Environmental Medical Biology, Arthropods of Medical Importance Resource Bank, Yonsei University College of Medicine, Seoul, Republic of Korea c Department of Parasitology and Medical Research Institute, Chungbuk National University School of Medicine, Cheongju, Republic of Korea d Department of Microbiology and Immunology, School of Medicine, Eulji University, Daejeon 301-746, Republic of Korea e Department of Parasitology and Tropical Medicine, Seoul National University College of Medicine, and Institute of Endemic Diseases, Seoul National University Medical Research Center, Seoul, Republic of Korea f Malaria Center, Provincial Health Department, Luang Prabang Province, Lao PDR g Department of Hygiene and Prevention, Ministry of Public Health, Vientiane, Lao PDR h Department of Parasitology, College of Medicine, Korea University, Seoul 136-705, Republic of Korea b

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Article history: Received 3 February 2014 Received in revised form 11 April 2014 Accepted 13 April 2014 Available online 20 April 2014 Keywords: Haplorchis taichui Haplorchis yokogawai Haplorchis pumilio Prevalence Metacercaria Lao PDR

a b s t r a c t This study confirmed the prevalence of the intestinal fluke Haplorchis taichui (Trematoda: Heterophyidae) among people and fish in Luang Prabang Province, Lao PDR. Fecal specimens were collected from 559 riparian people (229 males and 330 females), residing in 4 Districts (Luang Prabang, Xieng Ngeun, Pak Ou, and Nam Bak) and were examined by the Kato-Katz fecal smear technique. The overall helminth egg positive rate was 64.9%. The positive rate for small trematode eggs (STE), which may include H. taichui and other heterophyids, Opisthorchis viverrini, and lecithodendriids, was 15.2%. For recovery of adult helminths, 10 STE-positive people were treated with 40 mg/kg praziquantel and 15 mg/kg pyrantel pamoate, and then purged. Mixed infections with 3 Haplorchis species (H. taichui, H. pumilio, and H. yokogawai), a species of cestode (Taenia saginata), and several species of nematodes including Enterobius vermicularis and hookworms were found. The worm load for trematodes was exclusively high for H. taichui with an average of 7691 specimens per infected person, followed by H. yokogawai (8.3 specimens) and H. pumilio (4.1 specimens). Out of 207 freshwater fish (17 species) purchased in a market in Luang Prabang District, 138 (67%) harboured H. taichui metacercariae (metacercarial burden per fish; 520). Lower prevalence of fish and lower metacercarial density were observed for H. yokogawai (52% and 50 per fish, respectively) and H. pumilio (18% and 3 per fish, respectively). STE found in the surveyed population of Luang Prabang Province were verified to be those of intestinal fukes, particularly H. taichui. © 2014 Elsevier B.V. All rights reserved.

1. Introduction

∗ Corresponding author. Tel.: +82 2 740 8342; fax: +82 2 765 6142. E-mail addresses: [email protected] (W.-M. Sohn), [email protected] (T.-S. Yong), [email protected] (K.S. Eom), [email protected] (D.-Y. Min), [email protected] (D. Lee), [email protected] (B.-K. Jung), [email protected] (V. Banouvong), [email protected] (B. Insisiengmay), [email protected] (B. Phommasack), [email protected] (H.-J. Rim), [email protected], [email protected] (J.-Y. Chai). http://dx.doi.org/10.1016/j.actatropica.2014.04.020 0001-706X/© 2014 Elsevier B.V. All rights reserved.

Until the end of the 1990s, soil-transmitted nematodes (Ascaris lumbricoides, Trichuris trichiura, and hookworms) and the liver fluke (Opisthorchis viverrini) were the major helminth parasites prevalent among the people in Lao People’s Democratic Republic (Lao PDR) (Sornmani et al., 1974; Kobayashi et al., 1996; Chai and Hongvanthong, 1998; Rim et al., 2003). However, adult flukes of Haplorchis taichui, a heterophyid intestinal fluke, were recovered for the first time from 5 Laotian students studying in Czechoslovakia (Giboda et al., 1991). Thereafter, various minute intestinal flukes including Haplorchis spp. (H. taichui, H. pumilio, and H. yokogawai)

W.-M. Sohn et al. / Acta Tropica 136 (2014) 74–80

and lecithodendriids (Prosthodendrium molenkampi and Phaneropsolus bonnei) have been detected from the Laotian people (Chai et al., 2005a, 2007, 2009, 2010, 2013a; Sayasone et al., 2009). Centrocestus formosanus is another minute intestinal fluke species recovered recently from a few Laotians (Chai et al., 2013b). According to a 2000–2002 nationwide survey in Lao PDR, one of the characteristic epidemiological features for parasitic infections was that soil-transmitted helminths were highly prevalent in northern provinces (Huaphan, Luang Prabang, Oudomxay, Phongsaly, and Saysomboune), whereas liver and intestinal flukes were prevalent in southern regions (Savannakhet, Khammouane, Saravane, and Champasak) (Rim et al., 2003). Luang Prabang Province, located in the center of the northern part of Lao PDR, had a high prevalence of A. lumbricoides (65.2%) and Trichuris trichiura (71.0%) (Rim et al., 2003). However, at the same time, a 2.3% positive rate for small trematode eggs (STE) was recorded (Rim et al., 2003), which may include Opisthorchis viverrini, Haplorchis spp., and lecithodendriid flukes (Chai et al., 2005a, 2013a). It is of epidemiological importance to determine whether these STE are eggs of O. viverrini or those of minute intestinal flukes. In order to determine the responsible species, it is necessary to recover the adult flukes from the infected individual. The second intermediate host and the source of human infections for O. viverrini and Haplorchis spp. are freshwater fish. Therefore, information on the status of metacercarial infections in local fish is also essential. However, regarding the infection status in fish from Luang Prabang Province, only one study has been done by our team. In that 2004 study, the metacercariae of H. taichui, H. yokogawai, O. viverrini, and C. formosanus were first detected in 10, 6, 4, and 1 fish species, respectively (Rim et al., 2013). In February 2011, we surveyed helminth infections among people and fish in several districts of Luang Prabang Province, during the implementation of an international project entitled ‘Control of foodborne trematode infections among the Laotian people (2007–2011)’ under an agreement between Korea (Korea Foundation for International Healthcare) and Lao PDR (Ministry of Public Health). The study aimed to clarify the species of helminths infecting the riparian people of surveyed localities in Luang Prabang Province, Lao PDR. 2. Materials and methods 2.1. Surveyed areas and fecal examination The surveyed areas consisted of 10 riparian villages in 4 Districts (Luang Prabang, Xieng Ngeun, Pak Ou, and Nam Bak) of Luang Prabang Province, Lao PDR (Fig. 1). The river ‘Nam Ou’ runs through Pak Ou and Nam Bak Districts, and the river ‘Nam Khan’ flows through Xieng Ngeun and Luang Prabang Districts. The whole population of Luang Prabang Province was 455,532 as of 2011, and the population in the 4 Districts was estimated to be about 200,000. Most villagers were farmers or fishermen. Fecal samples, 559 in number, were collected from the village people (229 males and 330 females; 1 sample per person) 16–80 years of age. The fecal samples were transported to the laboratory of the Malaria Center, Provincial Health Department of Luang Prabang Province located in Luang Prabang City. The Kato-Katz thick smear technique was applied to detect helminth eggs (Table 1). STE were trematode eggs 20–35 ␮m in length, which may include eggs of O. viverrini, heterophyids, and lecithodendriids. 2.2. Recovery of adult flukes Ten STE and/or nematode egg-positive residents from Pak Chek Village, Pak Ou District, 25–53-years of age (3 men and

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7 women), who complained of variable degrees of abdominal discomfort and indigestion and agreed to this procedure were selected for anthelmintic treatment followed by purgation and adult worm recovery (Table 2). Informed consent was obtained from each resident, and the residents were treated with a single oral dose of 40 mg/kg praziquantel (Shinpoong Pharm, Seoul, Korea) in combination with 15 mg/kg pyrantel pamoate (Hangzhou Minseng Pharm, Hangzhou, China), and purged with 30–40 g MgSO4 . Whole consecutive diarrheic stools were collected 3–6 times over 4–5 h duration following purging, pooled individually, and processed as previously described (Chai et al., 2005a, 2007, 2009). Helminth specimens were collected and fixed in 10% formalin solution, stained with acetocarmine, and morphologically identified. Fecal examination and anthelmintic treatment of people were approved by the Ministry of Public Health, Lao PDR, under the agreement of the Korea-Laos International Collaboration. 2.3. Examination of fish We purchased 207 freshwater fish (17 species) from a market in Luang Prabang City in February 2011. It was stated that the fish were caught by fishermen from small streams in the suburbs of Luang Prabang City. The fish were refrigerated and transported to the Department of Parasitology and Institute of Health Sciences, Gyeongsang National University School of Medicine, Jinju, Korea. The fish species were identified with the aid of the FishBase website (http://www.fishbase.org/search.php). Artificial digestion (Han et al., 2008; Rim et al., 2008) was used to detect the metacercariae. The whole fish was ground in a mortar with a pestle, and digested with artificial gastric juice containing 0.6% pepsin (1:10000) and 0.8% HCl solution (conc.). After incubation at 37 ◦ C for 1 h, the digested mixture was washed with phosphate-buffered saline several times until the supernatant became clear. Trematode metacercariae were isolated from the sediment of the digested material using a stereomicroscope. The metacercariae were diagnosed based on size, shape, and other morphological characters. To determine the location of metacercariae in the fish body, some fish were subdivided into 3 parts (scales, head and gills, and flesh and fins), and each part was artificially digested. 2.4. Statistical analysis The differences in the prevalence of STE and hookworm eggs by different villages were statistically evaluated by the chi-square test. The p-values of

Prevalence of Haplorchis taichui among humans and fish in Luang Prabang Province, Lao PDR.

This study confirmed the prevalence of the intestinal fluke Haplorchis taichui (Trematoda: Heterophyidae) among people and fish in Luang Prabang Provi...
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