Diphyllobothrium latum

Diphyllobothriumlatum (Linnaeus, 1758) Cobbold, 1858

Figs 3-1 through 3-3

ETYMOLOGY:Di = two; phyllos = leaf, and bothrium = groove; along with latum from the Latin Lumbrici lati which was the term the Romans used to describe all tapeworms (as opposed to Lumbriciteretes for the earthworm).

SYNONYMS:Taenialata Linnaeus, 1758; Taeniavulgaris Linnaeus, 1758; Taeniamembranacea Pallas, 1781; Taeniatenella Pallas, 1781; Taeniadentata Batsch, 1786; Taeniagrisea Pallas, 1796; Bothriocephaluslatus (Linnaeus, 1758) Bremser, 1819; Dibothriumlatum (Linnaeus, 1758) Diesing, 1830; Bothriocephalusbalticus Küchemnmeister, 1855; Bothriocephaluscristatus Davaine, 1874; Bothriocephalustaenioides Léon, 1916; Dibothriocephalusminor Cholodlowsky, 1916; Diphyllobothriumamericanus Hall and Wigdor, 1918; DibothriumserratumDiesing 1850; Diphyllobothriumfuscum (Krabbe, 1865), Diphyllobothriumluxi (Rutkevich, 1937); Diphyllobothriumparvum Stephens, 1908; Diphyllobothrium stictus Talysin, 1932; Diancyrobothriumtaenioides Bacigalupo, 1945.

HISTORY: In 1592 Dunus was the first to recognizably describe Diphyllobothriumlatum; this description was confirmed by Plater in 1602, who differentiated it from the Taenia species (beef and pork tapeworms) of humans (Cited in Grove, 1990). The fish was shown to contain the stage that transmits the parasite to humans by Braun (1883) who fed plerocercoids from fish to cats, dogs, and medical students. The role of the copepod as the first intermediate host was elucidated by Janicki (1917) and Rosen (1917).

GEOGRAPHICAL DISTRIBUTION:Diphyllobothriumlatum has been reported to occur in humans throughout the world, in northeastern Europe, especially in Finland, Scandinavia,, the Baltic states, the former Soviet Union, France, and Switzerland. It is believed to have expanded its range at some point with human travels to Israel, central Africa, and Siberia. It was brought by Europeans to the Americas where foci were established in Canada, the Great Lakes of North America (although no longer present in most of the central United States (Peters et al., 1978), and Chile in South America (Torres et al., 1991). The worm in Japan may have been brought by Europeans or may represent a separate species, Diphyllobothriumnihonkaense Yamane, Kamo,, Bylund, and Wikgren, 1986. It has also been reported on occasion from the Phillippines and Taiwan. Infection in the domestic cat should parallel that in the human. Infection by a Diphyllobothrium latum has been reported in domestic cats in Scotland (Hutchinson, 1957), Russia (Vereta, 1986),India (Chandler, 1925?), Japan (Tanaka et al., 1985), Philippines (Tongson & San Pablo, 1979) and in Chile (Torres, et al., 1990).

LOCATION IN HOST: Adult Diphyllobothriumlatum are found in the small intestine of the cat. "The function of the scolex is to anchor the early strobila to the host gut wall. In the older worm, maintenance of position in the host gut is effected by muscular tonus, by pressure of the powerfully muscular strobila against the gut wall; the scolex serves little purpose, adheres only loosely to the gut wall, and any increase in its size and development is not to be expected.” (Wardle and Green, 1941).

IDENTIFICATION:Diphyllobothriumlatum is referred to as a diphyllobothriid tapeworm or as a Pseudophyllidean tapeworm. Common names include "the broad tapeworm” and "the broadfish tapeworm.” This tapeworm is often colloquially referred to as a "pseudotapeworm." The scolex of Diphyllobothriumlatum lacks hooks and suckers, but instead possesses two shallow, longitudinal grooves called bothria (Khalil et al., 1994). The scolex is 2.5 mm long and 1.0 mm wide (Figs 3-1 and 3-2).

Each proglottid of these tapeworms possess a centrally located, rosette-shaped uterus (Fig 3-3) and associated uterine pore through which its eggs are released (Faust, 1952). These tapeworms continuously release eggs until they become exhausted of their uterine contents. The terminal segments become senile rather than gravid and detach in chains rather than individually. In humans, this tapeworm may attain a length of 3 to 10 meters. This tapeworm may have as many as 3000 or more proglottids and may range in length from 2 to 12 meters. It is probable that this tapeworm does not attain this considerable length in the domestic cat.

The egg of Diphyllobothriumlatum resembles the egg of a digenetic trematode, that is, it is oval and possesses a distinct operculum at one pole of the shell. The eggs are light brown and have dimensions that average 67-71 µm by 40-51 µm. The eggs tend to be rounded at one end. The operculum is be present on the end opposite the rounded pole. The eggs are unembryonated when passed in the feces. The eggs can be distinguished form those of the Pseudophyllidean tapeworms of the genus Spirometra which also have a similar morphology in that the operculum is ellipsoidal in shape, the eggshell of Spirometra spp. tend to appear irregular because of the uneven curvature of the eggshell (Miyazaki, 1991).

LIFE CYCLE: Man serves as the principal definitive hosts for Diphyllobothriumlatum, although many other mammals that eat fresh-water fish (e.g., cat, dog, bear, and pig) may harbor the adult cestodes. In areas where human infection is rare or no longer present, infection of the fish intermediate hosts also becomes reduced or disappears, suggesting that wild mammalian hosts are not sufficient to maintain the cycle in many environments (Beaver et al., 1984). However, in areas of Russia where the infection is endemic, up to 90% of cats may be infected (Shamarina et al., 1980).

Unembryonated eggs pass through the uterine pore of each of the adult cestode's gravid proglottids. The eggs are discharged to the external environment with the feces. In fresh water, the first developmental stage, the ciliated coracidium, emerges from the egg and is eaten by the first intermediate host, an aquatic copepod (a crustacean). This copepod may be of the genera Cyclops or Diaptomus. The second developmental stage, the worm-like procercoid stage, develops within the copepod. When the procercoid is ingested by the second intermediate host, e.g., a fish such as a fresh-water fish, and the procercoid develops into a plerocercoid within the musculature of the fish. Cats become infected with Diphyllobothriumlatum by eating the fish and the plerocercoid develops to a mature tapeworm in the small intestine. Examination of the intestines of a kitten 13 hours after being fed plerocercoids recovered from fish, revealed the worms at distances of 7, 11, 12, 13, and 16 inches form the pylorus in a gut measuring 33 inches between pylorus and ileocolic valve; after 25 hours in another kitten, 17 worms were found between 7.5 and 36 inches behind the pylorus in a gut measuring 56 inches from pylorus to ileocolic valves (Wardle, 1933). In dogs, the first eggs are passed between 18 and 20 days after ingestion of the plerocercoid, and in some dogs, worms are a meter and a half long by 30 days after infection is initiated (Wardle and Green, 1941). In human beings, the worms may remain alive and active for several years or even decades, but the patent period in the cat has not been determined. With Diphyllobothriumlatum there is no clear distinction between mature and gravid proglottids, with maturation occurring sometimes anterior to less developed proglottids (Faust, 1952). Also, ultimate gravid proglottids are not "shed” in the feces as actively motile sacks of eggs as with Dipylidiumcaninum and Taeniataeniaeformis, but instead, as groups of segments become "spent”, they detach from the strobila and are shed as strands of variable length.

CLINICAL PRESENTATION AND PATHOGENESIS: As with many of the feline tapeworms, cases of diphyllobothriasis are apparently asymptomatic. Pet owners may observe chains of "spent" or empty proglottids in the cat's feces. Humans with this parasite demonstrate the same poorly defined symptoms as they do when infected with other tapeworms (vague abdominal discomfort, diarrhea, nausea and weakness). In humans, this parasite may produce a serious megaloblastic anemia. Virtually all of the cases have been in Finnish people. It has been estimated that almost a fourth of Finland's population may be infected with Diphyllobothriumlatum. About 10% of these will have pernicious anemia. The cestode does absorb large amounts of vitamin B12 and that affected humans also have an impaired ability to absorb this vitamin (von Bonsdorff, 1978). Pernicious anemia has not been reported in cats or any other domesticated or wild animals; however, the experimental infection of dogs with Diphyllobothriumlatum has induced decreased red cell numbers and decreases in total hemoglobin (Wardle et al., 1937).

DIAGNOSIS: Identification of characteristic eggs and "spent" proglottids as those of Diphyllobothrium latum is necessary for the practical requirements of controlling this cestode. Veterinarians must remember that the eggs of Diphyllobothriumlatum are operculated and resemble the eggs of Spirometra spp. and many of the digenetic trematodes.

Gross inspection with or without a hand lens is usually sufficient for the identification of proglottids of Diphyllobothriumlatum. Identification is based on the appearance of each proglottid's centrally located, rosette-shaped uterus and its associated genital pore. In cases of intact tapeworms recovered at necropsy, identification can also be made utilizing the characteristic appearance of the scolex with its slit-like bothria.

TREATMENT: Praziquantel must be administered at an elevated dose to be effective against Diphyllobothriumlatum. A single dose of 35 mg/kg body weight eliminated all Diphyllobothrium latum from infected dogs (Sakamoto, 1977).

EPIZOOTIOLOGY: Cats become infected when they eat raw or undercooked fish.

HAZARDS TO OTHER ANIMALS: In addition to cats, suitable hosts include a wide variety of various terrestrial and marine fish-eating carnivores (dogs, bears, mongoose, mink foxes, seals and sea lions) in many parts of the world. The stage passed in the feces of cats requires a period of development in fresh water, thus, infected cats pose no direct threat to other animals.

HAZARDS TO HUMANS: Human beings are considered to be the normal definitive host for Diphyllobothriumlatum. Because Diphyllobothriumlatum is a human tapeworm and because it may be transmitted to both wild and domesticated animals, it is considered to be a zooanthroponosis. The infected cat poses no direct threat to its owner or to any other individuals that may handle the cat or its feces.

CONTROL/PREVENTION: Prophylaxis involves the freezing or cooking of fish. At no time should cats be fed raw fish. Such habits may lead to infections with the infective plerocercoid stages of Diphyllobothriumlatum, and if possible, cats should not be allowed to roam freely or to scavenge dead fish (Hendrix and Blagburn, 1983). Precautions should be taken against raw human sewage reaching fresh water lakes in endemic areas; this has been a major cause of the infection of the stock of dish in lakes and rivers (von Bonsdorff, 1978).

REFERENCES

Beaver PC, Jung RC, Cupp EW. 1984. Clinical Parasitology, 9th edition. Lea & Febiger, Philadelphia, PA, USA. 825 pages.

Braun M. 1883. Bothriocephaluslatus und seine Herkunft. Arch pathol Anat Physiol lin Med (Virchow) 92:364-366

Chandler AC. 1925? The helminthic parasites of cats in Calcutta and the relation of cats to human helminthic infections. J Parasitol XX:213-227.

Faust EC. 1952. Some morphologic characters of Diphyllobothriumlatum. Anals Inst Med Trop 9:1277-1300.

Grove DI. 1990. A History of Human Helminthology. CAB International. Wallingford, UK, 848 pages.

Hendrix CM, Blagburn BL. 1983. Common gastrointestinal parasites. Vet Cl N Am 13:627-646.

Hutchison WM. 1957. The incidence and distribution of Hydatigerataeniaeformis and other intestinal helminths in Scottish cats. J Parasitol 43:318-321.

Janicki, C. 1917. Observations su quelques espèces de poissons afin d’arriver à connaître plus à fond le contenu de leour estomac et pour trover des stades encore inconnus de plerocercoide. Bull Soc Neuch Sci Nat 42:22-29.

Khalil LF, Jones A, Bray RA. 1994. Keys to the Cestode Parasites of Vertebrates. CAB International, Wallingford, UK, 751 pages.

Miyazaki I. 1991. Helminthic Zoonoses. Intl Med Found, Japan, Tokyo, 494 pages.

Peters L, Calvis D, Robertson J. 1978. Diphyllobothriumlatum currently present in northern Michigan? J Parasitol 68:999-1003.

Rosen F. 1917. Recherches sur le développement des Cestodes. I. Le cycle évolutif des Bothriocéphales. Etudes sur l’origine des cestodes et leurs états larvaires. Bul Soc Neuch Sci Nat 43:1-55.

Sakamoto T. 1977. The anthelmintic efficacy of Droncit on adult tapeworms of Hydatigerataeniaeformis, Mesocestoidescorti, Echinococcusmultilocularis, Diphyllobothriumerinacei, and D. latum. Vet Med Rev 1:64-74.

Shamarina AG, Kazantseva NA, Zavgorodnyaya NF, Balkov YM. 1980. The role of waterbodies in the spread of human diphyllobothriasis and opisthorchiasis in the Perm region. Biol Resu vodo sapad Urala. 145-147.

Tanaka H, Watanabe M, Ogawa Y. Parasites of stray dogs and cats in the Kanto region, Honshu, Japan. J Vet Med, Japan 771:657-661.

Tongson MS, San Pablo FG. 1979. A study on the prevalence of gastro-intestinal worms of cats in Metropolitan Manila. Philip J Vet Med 18:1-15.

Torres P, Ruiz E, Rebolledo C, Mira A, Cubillos V, Navarrete N, Gesche W, Montefusco A, Valdés L, Alberdi A. 1990. Parasitism in fish and human riverside communities from Huillinco and Natri Lakes (Great Island of Chiloé), Chile. Bol Chil Parasitol 45:47-55.

Torres P, Cubillos V, Gesche W, Rebolledo C, Montefusco A, Miranda JC, Arenas J, Mira A, Nilo M, Abello C. 1991. Difilobotriasis en salmonidos introducidos en lagos del sur de Chile: aspectos patologicos, relatcion don infeccion humana, animales domestics y aves piscivoras. Arch Med Vet 23:165-183.

Vereta LE. 1986. Helminths of cats in Moscow and epizootic aspects of some helminthiases. Bull Vsesoy Inst Gelmint, KI Skryabina 42:20-26.

von Bonsdorff B. 1978. The broad tapeworm story. Acta Med Scand 204:241-247.

Wardle RA. 1933. Significant factors in the plerocercoid environment of Diphyllobothrium latum (Linn.). J Helminthol 11:25-44.

Wardle RA, Green NK. 1941. The rate of growth of the tapeworm Diphyllobothriumlatum (L.). Can J Res 19:245-251.

Wardle RA, Gotschall MJ, Horder LJ. 1937. The influence of Diphyllobothriumlatum infestation upon dogs. Trans Roy Soc Can 31:59-69.

FIGURES:

Figure 3-1. Bothrium of Diphyllobothriumlatum showing the finger-like nature of the holdfast.

Figure 3-2. Bothrium of Diphyllobothriumlatum showing another view in which the holfast is twisted giving it a wider appearance.

Figure 3-3. Gravid segments of Diphyllobothriumlatum showing the branching uterus.

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