Diphyllobothriidae, Dipylidium and Hymenolepis Species

Description of the Pathogens

Pseudophyllidean cestodes in the family Diphyllobothriidae can cause intestinal tapeworm infections in humans. Around 16 species have been reported to cause human infections, though only six species have been confirmed with modern molecular techniques. In addition to humans, natural definitive hosts for the adult tapeworms generally include wild and domestic fish-eating terrestrial carnivores (e.g., dogs, cats, bears), marine mammals including pinnipeds, and some fish-eating birds. Infection usually is contracted by eating raw or undercooked fish. The first developmental stage occurs in crustaceans, and the second stage usually develops in fish; although for some Diphyllobothrium species, this second intermediate host is unknown.

In recent years, this group of tapeworms has undergone substantial taxonomic revision, and as a result, naming conventions have changed ( Table 279.1 ). Of note, the species formerly called Diphyllobothrium latum (fish or broad tapeworm) has been renamed Dibothriocephalus latus . Other primarily zoonotic tapeworms that can cause human infection include Dibothriocephalus nihonkaiense, Dibothriocephalus dendriticum, Adenocephalus pacificus, Diphyllobothrium stemmacephalum, and Diphyllobothrium balaenopterae . ^, The validity of some other sporadically reported species infecting humans, such as Dibothriocephalus ursi, Dibothriocephalus dalliae, and Dibothriocephalus alascencesis , requires investigation. On rare occasions, adult tapeworms of the genus Spirometra (also within the family Diphyllobothriidae) have been reported in human intestinal infections—this is distinct from sparganosis, a tissue-stage infection with larval Spirometra spp.

Diphyllobothriid adult-stage tapeworms attach to the small intestinal mucosa with two sucking grooves (i.e., bothria) located on the ventral and dorsal surfaces of the scolex (i.e., head). The body (i.e., strobila) of the tapeworm can reach up to the amazing length of 12 m. The strobila is composed of thousands of proglottid segments, which break off the distal end of the worm and are passed singly or in chains during defecation. Each proglottid contains thousands of eggs, some of which can be released into feces during passage through the intestinal tract. Feces must be deposited promptly into water for an egg to hatch and release a free-swimming embryo (coracidium).

The coracidium is ingested by copepods (including Cyclops and Diaptomus species), enters the body cavity, and develops into the first developmental stage (i.e., procercoid). If the copepod is ingested by plankton-eating fish, the second stage (plerocercoid) develops in the muscles . Depending on the parasite species, freshwater, anadromous, or marine fish are the second intermediate hosts ( Table 279.1 ). The second intermediate hosts for D. latus are freshwater fish such as pike, char, turbot, and perch. D. nihonkaiense is found in salmonid species in the Pacific Ocean. A. pacificus is found in marine fish from the Pacific coast of South America, and D. dendriticus has been reported in Atlantic salmon and whitefish. The major second intermediate or paratenic hosts for D. balaenopterae and D. stemmacephalum are not as clear, though Japanese anchovy and sardines have been implicated for D. balaenopterae and possibly other marine fishes and squid for D. stemmacephalum. Depending on the parasite species, the plerocercoids may develop in the muscle, viscera, or abdominal cavities of these fishes.

The plerocercoid develops into the adult intestinal tapeworm after the infected fish is ingested by an appropriate mammalian or avian host. For this group, definitive host specificity is low; for example, adult D. latus infections occur in humans, dogs, cats, foxes, bears, and pigs. Among the other species that occasionally infect humans, the natural definitive hosts are bears and sometimes other carnivores for D. nihonkaiense , pinnipeds (e.g., seals, sea lions) for A. pacificus, fish-eating birds (e.g., seagulls), and mammals for D. dendriticus, and marine mammals for D. balaenopterae and D. stemmacephalum (whales and dolphins respectively). ^,

Epidemiology

Diphyllobothriasis occurs worldwide and is primarily an infection of older children and adults, although infection of a 2-year-old child with D. nihonkaiense has been reported. Infection is most prevalent in populations whose culinary habits result in consumption of raw or undercooked fish flesh, liver, or roe.

Development of molecular tools to identify the Diphyllobothriidae genera and species that cause human infections provided insights into the epidemiology of this disease. In the past, most infections were attributed to D. latus, but later information based on molecular studies has implicated several other species. ^{, ,} Since molecular studies are limited in time and scope, it is difficult to define the true relative occurrence of D. latus infections versus other human-infecting species. Nonetheless, D. latus infections are most often reported in the temperate and subarctic zones of Eurasia, particularly Finland, Sweden, and Lithuania. D. latus and other Dibothriocephalus species occur in other populations of Europe (especially northern Italy, Romania, the lower Volga, and the Baltic nations), among indigenous peoples in Alaska and Canada, and in Latin America.

Human cases of A. pacificus infection have been reported mostly in Peru, Chile, and Argentina, though the distribution of the species in wildlife is broader and infections in other regions traced to imported fish have been identified. D. dendriticus is found in regions farther north than D. latus ; most infections in polar regions are likely caused by this species. Most human infections in Asia (Japan, Siberia, and Manchuria) are caused by D. nihonkaiense, though more recently, infections with this species have been recorded in North America and Europe via molecular testing. In the US, infected salmon has been implicated in 82% of 52 cases on the West Coast, suggesting these infections were most likely associated with D. nihonkaiense, given the preference for that species to parasitize Pacific salmon. ^, Fish from the Great Lakes region also have been implicated, although cases of diphyllobothriasis have been reported less frequently from this area in recent years. The two species still retained in the genus Diphyllobothrium, D. balaenopterae and D. stemmacephalum, appear to be mostly restricted to northern pacific regions of Japan, Korea, and Russia.

Because “fresh” fish are shipped nationally and internationally, the risk associated with consuming certain fish dishes (e.g., sushi, ceviche, lightly pickled fish, smoked fish, gefilte fish) is widespread, and human infections may be associated with nonnative Diphyllobothriidae. Parasites can be introduced into new regions as a result of aquaculture; one example is the possible introduction of D. latus to lakes in South America by means of plerocercoid infection in food fish species.

Clinical Manifestations

Few pathologic changes are observed in the intestinal mucosa of animals with diphyllobothriasis, and most infected people are asymptomatic. In a study in eastern Finland, 37% of the 295 tapeworm carriers had symptoms (vs. 8% of 832 controls) that included diarrhea, fatigue, change in appetite, and paresthesias; younger persons were less likely to have symptoms. Abdominal pain, nausea, and diarrhea occurred in 2 of 4 cases of diphyllobothriasis in a US outbreak associated with salmon sushi. All four family members involved in a more recent outbreak of D. nihonkaiense in Korea complained of abdominal pain and watery diarrhea.

Parts of the strobila can be passed in stool or vomitus, but proglottids are not very motile and do not spontaneously exit the anus, as can proglottids of the beef tapeworm Taenia saginata. Intestinal obstruction can occur when multiple worms are present. Megaloblastic anemia resulting from vitamin B ₁₂ deficiency is reported to occur in up to 2% of D. latus– infected Scandinavian adults. Pallor, fatigue, glossitis, decreased vibration sense, paresthesia, and central scotoma have been described as clinical features in these patients.

Laboratory Findings and Diagnosis

Mild eosinophilia (5%–15%) can occur. Intestinal diphyllobothriasis is diagnosed by finding typical eggs or discharged proglottids in feces at ≥5 weeks after ingestion of infected fish. Because egg discharge is intermittent in the intestinal diphyllobothriasis, the diagnosis can be missed if only single stool samples are examined. Eggs are colorless to light yellow and ovoid, with dimensions ranging from 40 to 80 μm. They are unembryonated (containing an undifferentiated morula) when passed in stool and have an indistinct operculum, which may open under coverslip pressure ( Fig. 279.1 ). Diphyllobothriid eggs must be differentiated from other medium to large-sized operculated eggs, such as those from the trematodes (flukes) Fasciola, Fasciolopsis, Echinostoma, Gastrodiscoides, Nanophyetus, and Paragonimus spp. Among the Diphyllobothriids, species identification based on egg morphology via light microscopy alone is not reliable due to interspecific size variability. Only a family-level diagnosis (i.e., Dihpyllobothriidae, or Dibothriocephalus/Adenocephalus/Diphyllobothrium ) should be reported unless the molecular analysis is undertaken for further identification. Though species identification is not necessary for treatment and management, it may be desired for epidemiological or research purposes.

The proglottids have a fleshy consistency and are ivory in color. The genital pore may appear as a central, raised darkened area. The proglottids are wider (12 mm) than they are long (4 mm). The appearance of these broad proglottids suggests the diagnosis of diphyllobothriasis, but a reliable species diagnosis is difficult without molecular methods, even when the proglottids and scolex are recovered and submitted to experts for examination. Although megaloblastic anemia is rare, up to 50% of tapeworm carriers in Finland were reported to have reduced serum vitamin B ₁₂ levels.

Treatment

For intestinal infections, single-dose therapy with praziquantel (5–10 mg/kg) is highly efficacious (i.e., 85%–95% cure rate); purgatives are not necessary. Niclosamide also is effective as a single dose, but it is no longer available in the US. Stool examinations to evaluate for cure may be performed 6 or more weeks after therapy. Cobalamin injections and oral folic acid are indicated for patients with clinical or laboratory evidence of vitamin B ₁₂ deficiency.

Prevention

Preventing these infections in humans depends on altering food handling and eating habits. Regulations for proper disposal of human feces alone have no impact on contamination of water supplies with eggs from animal sources. Cooking fish to an internal temperature of at least 63°C is recommended. Freezing at −35°C or below and storing at −20°C for 24 hours kills plerocercoids and renders the meat safe for consumption. Canned fish is safe, but smoked fish is safe only if the fish was frozen appropriately before smoking to kill any parasites. Although diphyllobothriasis is not transmitted from person to person, >1 family member may be infected when sharing common meals or if they have similar eating habits.