The Ecology of the Bithynia First Intermediate Hosts of Opisthorchis

Parasitology International 61 (2012) 38–45 Contents lists available at ScienceDirect Parasitology International journal homepage: www.elsevier.com/locate/parint The ecology of the Bithynia first intermediate hosts of Opisthorchis viverrini Trevor Petney a,⁎, Paiboon Sithithaworn b,c,⁎⁎, Ross Andrews b,c, Nadda Kiatsopit b,c, Smarn Tesana b,c, Carl Grundy-Warr d, Alan Ziegler d a Department of Ecology and Parasitology, Karlsruhe Institute of Technology, Kornblumenstrasse 13, Karlsruhe, Germany b Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, Thailand c Liver Fluke and Cholangiocarcinoma Research Center (LFCRC), Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, Thailand d Department of Geography, National University of Singapore, 21 Lower Kent Ridge Road, Singapore 119077 article info abstract Article history: Opisthorchiasis, together with its associated cholangiocarcinoma, is one of the most important human parasitic Received 28 February 2011 diseases on continental Southeast Asia. A great deal of epidemiological data from humans is available on this Received in revised form 14 July 2011 disease, particularly from the northeast of Thailand, however, only limited information is available on those Accepted 22 July 2011 aspects of the life cycle relating to its Bithynia (Gastropoda) and cyprinid fish intermediate hosts. Here we review Available online 29 July 2011 the information which is available on the Bithynia hosts of Opisthorchis viverrini. Only one major ecological study Keywords: has been carried out at one site on a single species of Bithynia. We show not only that detailed ecological studies Bithynia siamensis goniomphalos are required to clarify the epidemiology of opisthorchiasis, but also that the taxonomic status of the Bithynia Bithynia funiculata species transmitting O. viverrini requires clarification. Epidemiology © 2011 Elsevier Ireland Ltd. All rights reserved. Cercarial prevalence Habitat 1. Introduction Although the life cycle of O. viverrini has been known for many decades, few detailed studies have been carried out on its first and The trematode Opisthorchis viverrini is one of the most important second intermediate hosts. Many of these have been published in local human pathogens in the middle and lower Mekong area, comprising the journals and are therefore difficult to access. In addition, recent work north and northeast of Thailand, Lao PDR, Cambodia and southern on the genetic structure of geographically separated populations of O. Vietnam, where an estimated 67.3 million people are at risk of infection viverrini, as well as of its Bithynia first intermediate hosts suggests that [1]. Incomplete records from Thailand and Lao PDR indicate that over 9 both represent species complexes [4]. This work implies that any million people are infected, but as Thailand is the only one of these ecological study of the parasite or its hosts must take into account the countries with an adequate disease registration system this number is geographic origin of the samples [1]. Here, we provide a review of the likely to increase substantially as more information on prevalence, ecology of the Bithynia species which are involved in the life cycle of O. particularly from Cambodia and southern Vietnam, becomes available [1]. viverrini. O. viverrini has a complex life cycle (Fig. 1.) with eggs shed mainly by human hosts washing into freshwater habitats occupied by snail first 2. Bithynia taxa identified along the Lower Mekong? intermediate hosts belonging to the genus Bithynia. These snails eat the eggs and become infected. On maturity, the cercariae are released into Members of the genus Bithynia are known from fossil deposits in the water where they actively seek a fish host belonging to the family the Mae Moh Basin, northern Thailand dating back to the Middle Cyprinidae [2]. Once in these second intermediate hosts, the develop- Miocene some 13 million years ago [5,6]. Today, three Bithynia taxa mental cycle progresses to the metacercarial stage, after which potential are recognized from the Mekong area as first intermediate hosts of O. human and carnivore hosts become infected when they eat the infected viverrini: Bithynia funiculata from the north of Thailand, B. siamensis fish. Human infection occurs when raw, fermented or marinated fish, goniomphalos from Lao PDR and northeast Thailand to southern not adequately heated, is eaten [1]. Infection is common within the Vietnam including the Tonle Sap in Cambodia, and B. s. siamensis from Mekong area as such fish dishes make up a traditional part of the diet [3]. western and central Thailand, south of Mandalay in Myanmar, the Malaccan Peninsula, and south of the distribution of B. s. goniomphalos in Cambodia and southern Vietnam [7–9]. Another species, Bithynia ⁎ Corresponding author. Tel./fax: +49 721 60843913. pulchella, ranging from India to the north of Thailand has not been ⁎⁎Correspondence to: P. Sithithaworn, Department of Parasitology, Faculty of Medicine, associated with O. viverrini [7]. Khon Kaen University, Khon Kaen 40002, Thailand. Tel.: +66 43 348387; fax: +66 43 202475. The Lower Mekong River in Thailand, Lao PDR and Cambodia is E-mail addresses: [email protected] (T. Petney), [email protected] (P. Sithithaworn). recognized as a biodiversity hotspot for gastropod mollusks with ca. 1383-5769/$ – see front matter © 2011 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.parint.2011.07.019 T. Petney et al. / Parasitology International 61 (2012) 38–45 39 Fig. 1. The life cycle of Opisthorchis viverrini. 111 recognized endemic species [10,11]. Davis [10] points out that Bithynia (Digoniostoma) siamensis containing 2 subspecies B. s. siamensis gastropod species often have abutting or barely disjunct demes and B. s. goniomphalos. Gabbia has now been raised to generic status probably with little or no gene flow between them. [12,13].Brandt[7] indicated that future studies would be likely to alter this taxonomic situation as many species in the family Bithyniidae were “Considering the habitat complexity and width of the 300 mile still anatomically unknown. Chitramvong [14,15] has now provided stretch of river that also includes major tributaries, and the more detailed anatomical and morphological analyses, although only a patchiness and small area of species and deme patches through- single sample (population) was used for each species. out this area, it is highly probable that speciation has taken place Recently, a number of new species of Bithynia have been described in this centre as habitats evolved and diversity increased.” [10]. elsewhere, with the authors suggesting that the genus is more diverse than previously realized [16–18]. This can be related to their low This is an ongoing process. ability to disperse and small species ranges [19], fitting closely Davis' Of the ca. 130 species in the genus Bithynia worldwide, about 25 pattern for gastropod speciation along the Mekong. occur in the Oriental Region [11].Brandt[7] recognized two subgenera The Bithynia taxa which act as intermediate hosts of O. viverrini have from Thailand, Gabbia and Digoniostoma, containing 3 species each, with all been characterized, and are identified, on the basis of morphological 40 T. Petney et al. / Parasitology International 61 (2012) 38–45 making up the intermediate hosts of O. viverrini. As the genetically distinguishable populations of the intermediate hosts of O. viverrini occur in different wetland systems, an analysis of ecological patterns must take the origin of specimens into account. 3. Recent distribution records of the Bithynia intermediate hosts of O. viverrini in Thailand Recent work has shown the almost exclusive presence of B. funiculata in the north of Thailand, B. s. siamensis in the central area and B. s. goniomphalos in the northeast (Table 1). This mirrors the regions sampled with most research being concentrated in areas already well characterized. The major exception to this scheme is the seminal paper on the mollusks of Thailand by Brandt [7] which shows a much broader distribution for B. s. siamensis including northern, western and southeastern Thailand with considerable areas of sympatry with B. funiculata, with which it was collected. This strongly suggests that the selective sampling of locality carried out to date provides biased information at least for B. s. siamensis. 4. Habitat choice The Bithyniidae are generally dwellers of slow flowing, muddy rivers, artificial and natural ponds, lakes, irrigation canals and swamps [24]. Bithynia s. goniomphalos is no exception, occupying a wide variety of such habitats including temporary and permanent freshwater bodies, shallow ponds, marshes, reservoirs and irrigation canals [7,14] (Fig. 3). They can be found on and in the mud, on rocks as well as on vegetation [25]. In Lao PDR, B. s. goniomphalos appears to be the most common species in paddy fields [26] and reservoirs, while B. s. siamensis is more commonly found in irrigation canals and drainage Fig. 2. Snail host of O. viverrini in Southeast Asia. a. Bithynia funiculata.b.B. siamensis ditches with flowing water and artificial ponds [26]. Chitramvong [15] goniomphalos.c.B. s. simensis. indicates that B. s. siamensis prefers a substrate of algae or other water plants such as lotus leaves. Giboda et al. [26] indicate that B. s. laevis, characteristics [7,15] (Fig. 2). A recent molecular taxonomic study, which is considered to be a synonym of B. s. siamensis by Brandt [7],is however, has shown that B. s. goniomphalos from the northeast of an “ecological form” of B. s. goniomphalos found in running water Thailand and Lao PDR show considerable genetic variability with where it occurs together with B. s. siamensis in such habitats [27]. populations from different wetlands being genetically distinct [4].The Thammasiri et al. [28] mention unpublished data showing that B. s. degree of genetic differentiation suggests that at least 2 species are goniomphalos can occur at a depth of 3 m, while Tesana [29] indicates present. In a follow-up study using multilocus enzyme electrophoresis, that it is found at all depths up to 10 m, but not at depths below 12 m.

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