Opisthorchiidae

Siberian liver fluke Opisthorchis felineus, from the Center for Disease Control and Prevention.

Belongs within: Opisthorchioidea.

The Opisthorchiidae are flukes found in the gall bladder and bile ducts of tetrapods (Dawes 1956).

Depending on the liver
Published 28 July 2016
Stained specimen of Asian liver fluke Clonorchis sinensis, from here.

Every year, tens of millions of people worldwide (particularly in tropical Asia) suffer the effects of clonorchiasis and opisthorchiasis, conditions caused by infections with liver flukes of the family Opisthorchiidae. Exactly which condition the victim is suffering from depends on just which species of flukes they find themselves infected with, but there is little immediate difference between the clinical symptoms of either. Issues arising from clonorchiasis include fever, jaundice, diarrhoea and malnutrition. Long-term or heavy infections may result in cirrhosis, pancreatitis or even cancer (King & Scholz 2001). But just what is responsible for these debilitating illnesses?

Flukes are a diverse group of endoparasitic flatworms that reach maturity in association with vertebrates. As with other parasite lineages, different fluke species prefer different hosts and infect different parts of the host’s system. Many have complex life cycles involving multiple larval stages and the successive infection of up to three distinct hosts on the way to maturity. Opisthorchiidae have such a three-host life cycle; their adult (or ‘definitive’) hosts span the gamut of vertebrates from fish to birds to mammals. Opisthorchiids in the strict sense are invariably associated with the liver of these hosts, taking up residence in the bile duct and gall bladder (however, phylogenetic studies have indicated that the closely related Heterophyidae, which infect the intestine, are probably paraphyletic with regard to opisthorchiids and the two families may be merged into an expanded Opisthorchiidae—Thaenkham et al. 2012). When mature they are elongate and flattened with the mouth near the front of the body surrounded by a sucker for attachment to host tissue. A second sucker is present on the underside of the body not too far behind the first (Dawes 1956).

Like other internal parasites, liver flukes are incredibly fecund. A female of Clonorchis sinensis, one of the main opisthorchiid species of concern to humans (yes, flukes reproduce sexually; I’ll allow a moment for the disgusting implications to fully sink in), may produce up to 4000 eggs in a single day. These eggs are released into the host’s digestive system, passing out in the faeces. They do not hatch until after they are ingested by the first larval host, an aquatic snail (many sources will say a freshwater snail but at least one opisthorchiid genus, Delphinicola, paratises marine dolphins so presumably has a correspondingly marine gastropod host). The egg hatches into a ciliated larva called a miracidium that over the course of the next few hours will find a likely spot in the snail’s gut to develop into the next larval stage, the sporocyst. The sporocyst is immobile and mouthless, and feeds by absorbing nutrients directly from the host tissue. It also contains a mass of germ tissue that develops into multiple individuals of the next larval stage, the redia, that are released from the parent sporocyst after a couple of weeks or so. The rediae are worm-like and mobile, chomping their way through suitable sections of host tissue. They also develop multiple individuals of the next stage within them just as the sporocysts did. In this way, a single egg may eventually result in an exponentially increased number of larvae.

Life cycle of Clonorchis sinensis, from here.

The next larval stage is called the cercaria. In opisthorchiids, the cercariae look a bit like tadpoles with a dorsoventrally finned tail. I haven’t found exactly how opisthorchiid cercariae are released into the water column but in other flukes they may be released with the discharge from the abcess or cyst that forms as the rediae feed on their host, or escape from the host tissue after the snail dies as a result of its infection. The cercaria is a dispersive stage that seeks out the next host in the life cycle. This they do by hanging head-down in the water column and allowing themselves to slowly sink until disturbed by contact with a potential host or water-currents created by its movement. At this point the cercaria rapidly swims upwards before allowing itself to sink again, hopefully onto the new hosts skin. The cercaria will then dig its way into the host’s muscle tissue and transform into the last larval stage, a cyst called a metacercaria. Opisthorchiid cercariae most commonly attach themselves to some kind of fish but they are a bit less picky about their host than the other stages in their life cycle; opisthorchiid metacercariae have also been found in crustaceans and have been shown in the laboratory to even be capable of infecting mammals (specifically guinea pigs).

The developing liver fluke reaches its definitive host when the second larval host is eaten. A young fluke hatches from the metacercaria inside the definitive host’s gut and make their way to the liver which they find by detecting the traces of its chemical products and/or by detecting the physical track of the bile duct. There they will mature into fully adult flukes, all ready to begin the cycle again (by doing the nasty in some poor sod’s gall bladder).

The economic impact of opisthorchiids around the world is estimated to amount to hundreds of millions of dollars each year. Unfortunately, as with many other illnesses more widespread in developing nations, there still remains a lot to be learned about their control. Cooking fish before consumption to kill metacercariae is one of the more obvious methods, though it should be noted that metacercariae can be devillishly difficult buggers to kill. Installation of sanitation and sewerage systems can also help by reducing the chance of egg-carrying faeces to make it into water bodies, though medically significant opisthorchiids may also infect animals other than humans such as cats, dogs or pigs. For now, it looks like liver flukes will be with us for some time.

Systematics of Opisthorchiidae

Characters (from Dawes 1956): Elongate, flattened, lanceolate distomes of delicate appearance, with weakly developed, closely approximated suckers. Genital ducts with cirrus small, vesicula seminis coiled, cirrus pouch absent, genital pore median, slightly in front of ventral sucker. Testes situated in posterior part of body and of variable shape, ovary in front of testes. Vitellaria follicular, lateral, generally situated in front of gonads. Excretory vesicle Y-shaped, with long stem and short lateral canals that do not extend beyond level of ovary anteriorly. Flame-cell formula variable. Uterus with folds mainly confined to region in front of ovary. Eggs numerous, small, light brown, each containing a larva. Hosts reptiles, birds, mammals; located in gall bladder and bile ducts. Cercariae gymnocephalous. Larvae encysted in fishes and amphibians.

Opisthorchiidae [Opisthorchidae]
| i. s.: Ratzia parvaD56
| Omphalometra flexuosaD56
|--OpisthorchiinaeD56
| |--CyclorchisD56
| |--CladocystisD56
| |--Amphimerus Barker 1911 [incl. Paropisthorchis Stephens 1912]D56
| | |--‘Opisthorchis’ caninus Barker 1911 [=Paropisthorchis caninus]D56
| | |--A. lancea (Diesing 1850)D56
| | |--A. novocerca (Braun 1902) [=Opisthorchis novocerca]D56
| | |--A. ovalisOC03
| | `--A. speciosus (Stiles & Hassall 1896)D56
| `--Opisthorchis Blanchard 1895 (see below for synonymy)D56
| |--O. asiaticus (Skrjabin 1913)D56
| |--‘Cercaria’ chromatophila Lebour 1914D56
| |--O. entzi Ratz 1900D56
| |--O. felineus (Rivolta 1884) (see below for synonymy)D56
| |--O. geminus (Looss 1896) [=Distomum geminum, O. gemina; incl. O. geminus var. kirghisensis Skrjabin 1913]D56
| |--O. pedicellataD56
| |--O. simulans (Looss 1896) (see below for synonymy)D56
| |--‘Clonorchis’ sinensis (Cobbold 1875)B96 [incl. C. endemicusPB27]
| |--O. skrjabini Zhukova 1934D56
| `--O. tenuicollis (Rudolphi 1819) (see below for synonymy)D56
`--MetorchiinaeD56
|--Parametorchis Skrjabin 1913D56
|--Holometra Looss 1899D56
| `--H. exigua (Mühling 1898) [=Distoma exiguum, Opisthorchis exigua]D56
|--Pseudamphistomum Lühe 1909D56
| |--P. danubiense Ciurea 1913D56
| `--P. truncatum (Rudolphi 1819) (see below for synonymy)D56
|--Metorchis Looss 1899D56
| |--M. albidus (Braun 1893) [=Distoma albidum, Opisthorchis albidus]D56
| |--M. crassiusculus (Rudolphi 1809) (see below for synonymy)D56
| |--M. tener (Kowalewsky 1898)D56
| |--M. xanthosomus (Creplin 1846) [=Distoma xanthosomum, Opisthorchis xanthosoma]D56
| `--M. zakharovi Layman 1922D56
`--Pachytrema Looss 1907 [Pachytrematinae]D56
|--P. calculus Looss 1907D56
|--P. hewlettiD56
|--P. magnum Travassos 1921D56
|--P. paniceum Brinkmann 1942D56
|--P. proximum Travassos 1921D56
|--P. sanguineum (Linton 1928)D56
`--P. tringae Layman 1926D56

Metorchis crassiusculus (Rudolphi 1809) [=Distoma crassiusculum, Opisthorchis crassiuscula; incl. O. xanthosomus var. compascuus Kowalewsky 1898]D56

Opisthorchis Blanchard 1895 [=Opiscorcus (l. c.), Opisthorchic (l. c.), Opistorchis (l. c.); incl. Clonorchis Looss 1907, Gomtia Thapar 1930, Notaulus Skrjabin 1913, Prosthometra Looss 1896]D56

Opisthorchis felineus (Rivolta 1884) [=Distoma felineum, Campula felinea, Dicrocoelium felineus, Opisthorchis tenuicollis felineus; incl. Distoma lanceolatum canis familiaris Tright 1889, D. conus Gurlt 1831 non Creplin 1825, D. lanceolatum felis cati Siebold 1836, D. sibiricum Winogradoff 1892, Opisthorchis wardi Wharton 1921, D. winogradoffi Jaksch 1897]D56

Opisthorchis simulans (Looss 1896) [=Distoma simulans, O. longissimus simulans; incl. O. simulans var. poturzycensis Kowalewsky 1898]D56

Opisthorchis tenuicollis (Rudolphi 1819) [=Distoma tenuicollis; incl. D. viverrini Poirier 1886, Opisthorchis viverrini]D56

Pseudamphistomum truncatum (Rudolphi 1819) [=Amphistoma truncatum, Distoma truncatum, Metorchis truncatus, Opisthorchis truncatus; incl. Distoma campanulatum Ercolani 1875, D. conus Creplin 1825]D56

*Type species of generic name indicated

References

[B96] Bond, C. E. 1996. Biology of Fishes 2nd ed. Saunders College Publishing: Fort Worth.

[D56] Dawes, B. 1956. The Trematoda with special reference to British and other European forms. University Press: Cambridge.

King, S., & T. Scholz. 2001. Trematodes of the family Opisthorchiidae: a minireview. Korean Journal of Parasitology 39 (3): 209–221.

[OC03] Olson, P. D., T. H. Cribb, V. V. Tkach, R. A. Bray & D. T. J. Littlewood. 2003. Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology 33: 733–755.

[PB27] Pilsbry, H. A., & J. Bequaert. 1927. The aquatic mollusks of the Belgian Congo, with a geographical and ecological account of Congo malacology. Bulletin of the American Museum of Natural History 53 (2): 69–602, pls 10–77.

Thaenkham, U., D. Blair, Y. Nawa & J. Waikagul. 2012. Families Opisthorchiidae and Heterophyidae: are they distinct? Parasitology International 61: 90–93.

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