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Discovery of Carcinogenic Liver Fluke Metacercariae in Second International Journal of Environmental Research and Public Health Article Discovery of Carcinogenic Liver Fluke Metacercariae in Second Intermediate Hosts and Surveillance on Fish-Borne Trematode Metacercariae Infections in Mekong Region of Myanmar Ei Ei Phyo Myint 1, Amornpun Sereemaspun 2, Joacim Rocklöv 3 and Choosak Nithikathkul 1,* 1 Tropical and Parasitic Diseases Research Unit, Graduate Studies Division, Faculty of Medicine, Mahasarakham University, Mahasarakham 44000, Thailand; [email protected] 2 Department of Anatomy, Faculty of Medicine, Chulalongkorn University, Bangkok 10330, Thailand; [email protected] 3 Department of Public Health and Clinical Medicine, Section of Sustainable Health, Umeå University, SE–901 87 Umeå, Sweden; [email protected] * Correspondence: [email protected]; Tel.: +668-14-03-8562 Received: 21 April 2020; Accepted: 30 May 2020; Published: 9 June 2020 Abstract: Countries of lower Mekong regions are highly alarmed by the spread of fish-borne trematode infections, i.e., small liver flukes and minute intestinal flukes especially in Thailand, Lao People’s Democratic Republic (Lao PDR), Vietnam, Cambodia and Myanmar. Moreover; the incidence of cholangiocarcinoma has also been increasing in the endemic area of liver fluke infections. Only a few reports have been published concerning the fish-borne trematodes infections in the central region of Myanmar. However; there is still a lack of information regarding the status of trematodes infections in second intermediate hosts in the Mekong region of Myanmar. Therefore, we conducted surveillance on the distribution of trematode metacercariae in small cyprinoid fishes collected from the Mekong region of Myanmar. A total of 689 fishes (12 different species of cyprinoid fishes) have been collected and examined by pepsin digestion methods. We discovered four species of fish-borne trematode metacercariae infections, i.e., carcinogenic liver fluke, Opisthorchis viverrini; minute intestinal flukes, Haplorchis taichui; Haplorchis pumilio and Haplorchoides sp. in Tachileik, the Mekong Region of Myanmar. The outcome of this study could be a useful index for the fish-borne zoonotic trematode epidemiology in the Mekong area. Besides, the results of our study contribute to filling the gap of information necessary for the control and prevention of fish-borne trematode zoonotic infections in the Mekong region. Keywords: opisthorchiidae; opisthorchis viverrini; minute intestinal flukes (MIF); Heterophyidae 1. Introduction The important public health problem of the spread of fish-borne trematodes (FBT) has highly alarmed the countries of the lower Mekong basin especially Thailand, Lao People’s Democratic Republic (Lao PDR), Cambodia, Vietnam and Myanmar [1–5]. Fish-borne zoonotic trematodes (FZT) especially small liver flukes (Opisthorchiidae) and minute intestinal flukes (Heterophyidae) are highly prevalent in those regions [6]. These two flukes have similar life cycles involving two intermediate hosts [7,8]. The first intermediate hosts are snails, and the second intermediate host are small freshwater fishes [9,10]. Humans are infected through ingestion of undercooked or raw freshwater fishes, which are contaminated with the infective stage of the parasite, i.e., metacercariae [11]. The traditional habit of eating raw or undercooked fish is a known risk factor for human trematode Int. J. Environ. Res. Public Health 2020, 17, 4108; doi:10.3390/ijerph17114108 www.mdpi.com/journal/ijerph Int. J. Environ. Res. Public Health 2020, 17, 4108 2 of 12 Int. J. Environ. Res. Public Health 2020, 17, x 2 of 12 trematodeinfections infections [7]. Opisthorchiasis [7]. Opisthorchiasis caused by carcinogeniccaused by carcinogenic liver fluke, Opisthorchisliver fluke, Opisthorchis viverrini, is an viverrini, important is anpublic important health public problem health in lowerproblem Mekong in lower region Mekong countries region [12 countries–19]. Heterophyiasis [12–19]. Heterophyiasis is an infection is an of infectionthe small of bowel, the small which bowel, is caused which by is minute caused intestinal by minute flukes intestinal (Heterophyidae) flukes (Heterophyidae) [20–23]. The incidence[20–23]. Theof cholangiocarcinomaincidence of cholangiocarcinoma has also been increasinghas also been in the increasing endemic in area the of endemic liver fluke area infections of liver [fluke24,25 ]. infectionsIn Myanmar, [24,25]. there In isMyanmar, one report there in 2019 is one about report a retrospective in 2019 about study a retrospective of the cholangiocarcinoma study of the cholangiocarcinomacases admitted to the cases Hepatobiliary admitted to and the Hepatobi Pancreaticliary surgery and Pancreatic department, surgery Yangon department, Specialty Hospital,Yangon SpecialtyMyanmar, Hospital, which shows Myanmar, that thewhich prevalence shows that has notablythe prevalence been increasing has notably since been 2016, increasing and the highest since 2016,prevalence and the was highest in 2018 prevalence [26]. Myanmar was in 2018 people [26]. alsoMyanmar have thepeople traditional also have habit the oftraditional eating raw habit small of eatingcyprinoid raw fishes small pickled cyprinoid with rice,fishes locally pickled called with (Nyar rice, lay locally Chin) (Figurecalled 1(Nyar). Moreover, lay Chin) infection (Figure can also1). Moreover,occur via poorinfection personal can also hygiene occur and via the poor contamination personal hygiene of food, and hands the contamination and food preparation of food, utensilshands andthat food are contaminatedpreparation utensils with metacercariae that are contaminated [27–30]. For with the increasing metacercariae data of[27–30]. cholangiocarcinoma For the increasing cases datafrom of Myanmar, cholangiocarcinoma the associated cases risk factorsfrom Myanmar, such as carcinogenic the associated liver flukerisk factors infection such and as epidemiological carcinogenic liverdata fluke require infection more surveillance and epidemiological for the control data and require prevention. more surveillance In the central for region the control of Myanmar, and prevention.seven species In the of minutecentral region intestinal of Myanmar, flukes (members seven species of the of Heterophyidae) minute intestinal have flukes been (members reported of in theYangon, Heterophyidae) Myanmar [have5]. However, been reported there isin stillYangon, a lack Myanmar of information [5]. However, about the there fish-borne is still trematodea lack of informationinfection status about from the thefish-borne Mekong trematode region of infectio Myanmar.n status Tachileik from the is a Mekong town situated region inof theMyanmar. Mekong Tachileikbasin of Myanmaris a town situated (Figure2 in). Geographically,the Mekong basin the of city Myanmar is also situated(Figure 2). in theGeographically, Golden Triangle the city that is is alsothe areasituated where in thethe bordersGolden of Triangle Thailand, that Laos is andthe Myanmararea where meet the atborders the confluence of Thailand, of the Laos Ruak and and MyanmarMekong rivers.meet at Therefore, the confluence we conducted of the Ruak a survey and Mekong on trematode rivers. matercerceriaeTherefore, we conducted infections a in survey second onintermediate trematode matercerceriae hosts from Tachileik, infections Mekong in second region intermediate of Myanmar, hosts and from we Tachileik, believe that Mekong our data region will ofprovide Myanmar, required and we epidemiological believe that our information data will topr fillovide the required knowledge epidemiological gap and provide information valuable datato fill to thesolve knowledge the public gap health and problem provide of valuable control anddata prevention to solve the of fish-bornepublic health trematode problem zoonotic of control infections and preventionin countries of offish-borne the Mekong trem basin.atode zoonotic infections in countries of the Mekong basin. FigureFigure 1. 1. PhotosPhotos of of local local Myanmar Myanmar food food (a ()a )Raw Raw small small cyprinoid cyprinoid fishes fishes pickled pickled with with rice rice (Nyar (Nyar lay lay Chin)Chin) (b (b) )Nyar Nyar lay lay Chin Chin prepared prepared as as an an uncooked uncooked salad salad mixed mixed with with onion onion (Nyar (Nyar lay lay Chin Chin salad) salad).. 2. Material and Methods 2. Material and Methods 2.1. Collection of Cyprinoid Fishes and Identification of Fish Species 2.1. Collection of Cyprinoid Fishes and Identification of Fish Species A total of 689 fishes (12 different species of cyprinoid fishes) were purchased from local markets in Tachileik,A total lower of 689 Mekong fishes (12 region differen of Myanmart species (Tableof cyprinoid1). Tachileik fishes) is were a town purchased situated infrom the Mekonglocal markets basin inof Tachileik, Myanmar lower (Figure Mekong2), which region is also of situatedMyanmar in (Table the Golden 1). Tachileik Triangle is that a town is the situated area where in the the Mekong borders basinof Thailand, of Myanmar Laos and(Figure Myanmar 2), which meet is atalso the situated confluence in the of theGolden Ruak Triangle and Mekong that is rivers. the area The where cyprinoid the bordersfishes were of Thailand, collected Laos from and January Myanmar 2018 tomeet December at the confluence 2019. All collected of the Ruak fishes and were Mekong transferred rivers. on The ice cyprinoidto the laboratory fishes were of the collected Department from of January Medicine, 201 Mahasarakhum8 to December University.2019. All collected The length
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