Tapeworms (Cestodes)

Parasite Life Cycle

The parasitic cestodes discussed in this chapter are flatworms (platyhelminths) of the orders Pseudophyllidea ( Diphyllobothrium and Spirometra ) and Cyclophyllidea (other species), which divide their life cycle between two animal hosts ( Fig. 289.1 ). As mature tapeworms, these parasites reside in the intestinal tract of a definitive host, a carnivorous mammal. Depending on the parasite species, mature tapeworms vary in length from several millimeters ( Echinococcus spp.) to 25 m (Diphyllobothrium) .

The tapeworm consists of a head (scolex) , a neck, and a tail. The head has two or more suckers and in some cases a rostellum, or knob of small hooks, used to attach to the wall of the host's intestine ( Fig. 289.2A ). The scolex is connected by a short neck to the lower portion of the tapeworm, the strobila, which is a ribbon-like chain of independent but connected segments called proglottids ( Fig. 289.2B ). Each proglottid has both male and female sexual organs and is responsible for producing the parasite's eggs. Proglottids begin to develop in the neck region of the parasite and then mature and move downward in the strobila as new segments are added from above. The hermaphroditic proglottids become gravid and eventually break free of the tapeworm. Proglottids may degenerate in the stool, releasing eggs (thousands to millions per day) into the feces. Alternatively, intact proglottids may be passed in the stool, with egg release occurring outside the body. In some cases, a section of strobila may be passed in a single day, with no further release of proglottids for several days thereafter. In practical terms, this means that although the number of tapeworm eggs in the stool is usually high, detection of parasite eggs by standard stool examination may be sporadic. Therefore multiple stool samples, rectal swabs, and visual examination of stool and perineum for proglottids may be required to detect a tapeworm infection. For some species of tapeworm (e.g., T. saginata ), the proglottids are motile. They may migrate within the gastrointestinal tract, causing biliary or appendiceal obstruction, or out of the body, to be found in the perineum.

At the point at which eggs are released, two effective biotypes of parasite can be defined. If the eggs released from the parasite are partially developed, they are called embryonated. If the egg embryo has not yet begun its differentiation, the egg is referred to as nonembryonated. In biologic terms, the embryonated egg can immediately infect the next intermediate mammalian or insect host, typically a herbivore or omnivore, through ingestion of food containing the egg. Such eggs, typical of Echinococcus spp., Taenia spp., and H. nana, may lie dormant in grazing areas or become scattered in the home environment and remain infectious for several months to years. Once ingested, the egg hatches in the intermediate host's intestine, releasing an oncosphere, which penetrates the gut mucosa to reach the circulation. The oncosphere passes to any of several organs to form a parasite cyst, which is variously called a cysticercoid, cysticercus, alveolar cyst, or hydatid cyst, depending on its morphology. The life cycle of these parasites is completed when the carnivorous definitive host consumes the cyst-infected tissues of the intermediate host and the cyst develops into a mature tapeworm in the lumen of the definitive host's intestine.

For nonembryonated eggs, such as those of the fish tapeworm D. latum, initial development takes place outside the body in water, after which the eggs hatch to release a free-swimming coracidium larva. In time, the coracidium is ingested by a small crustacean called a copepod and then develops into a procercoid larva within the copepod's tissues. When the copepod is ingested by a fish or other intermediate host, the procercoid infects its musculature, developing into the next larval stage, the plerocercoid cyst, or sparganum. If an uncooked plerocercoid of D. latum is ingested by a human, its definitive host, it develops into a mature, intraluminal fish tapeworm. However, if the fish containing the plerocercoid is ingested by another, larger fish, it does not become a tapeworm. It reencysts instead as a plerocercoid in the muscles of the second, larger fish.

Plerocercoid encystment or reencystment is significant in terms of human disease (as sparganosis ) for cestode species for which humans cannot serve as the definitive host (e.g., Spirometra mansonoides, a tapeworm of dogs and felines). Plerocercoids can develop in human tissues if Spirometra -infested copepods are ingested in drinking water. Alternatively, human plerocercoid cysts may be acquired via the intestine from another intermediate host (e.g., tadpole, frog, snake) if the meat of that aquatic host is eaten uncooked. Migrating plerocercoid cysts can also transfer directly into the skin or the eye if raw flesh of an aquatic intermediate host is used as a poultice in traditional healing.

As a rule, humans are either definitive or intermediate hosts for a given cestode parasite, but not both. For example, humans are solely definitive hosts (i.e., with tapeworms) for D. latum (fish tapeworm) and T. saginata (beef tapeworm) and are solely intermediate hosts for Echinococcus spp. (hydatid cysts and alveolar cysts), Spirometra (sparganosis), and T. multiceps (coenurosis). There are two exceptions to this rule. The first is T. solium, which develops in humans as a cysticercus if ingested as an egg or as a tapeworm if ingested as a cysticercus in infected pork. It is thus possible for one patient to harbor both cyst and tapeworm forms of T. solium. Such dual infection is seen in approximately 25% of cysticercosis cases. The second exception is the dwarf tapeworm, H. nana, whose eggs, after ingestion, hatch in the gut and encyst within the wall of the human intestine. After 5 to 7 days, the cyst breaks open, and the larva develops (within the same host) to become a mature tapeworm. The fertile eggs of this tapeworm may directly infect the mucosa, permitting a continued increase in the number of tapeworms in the affected host, without further exposure to environmental egg contamination. In this manner, humans serve as both intermediate and definitive hosts for H. nana. Single-host proliferation such as that of H. nana is highly unusual among human cestode infections and helminth infections in general. Normally, heavy cestode infections can be acquired only by repeated environmental exposure to eggs or infectious parasite cysts.

Disease Pathogenesis and Immunology

Adult tapeworms in the intestinal tract generally cause minimal local pathology. Reduced nutrient absorption and alteration of gut motility have been described, but there is no firm association of adult tapeworm infection with specific bowel symptoms. An immune response to adult tapeworms provokes eosinophilia and immunoglobulin E (IgE) elevation in some patients, but the immune response does not appear to alter the course of an intraluminal tapeworm infection. In light of the limited range of potential hosts observed for most adult tapeworms, it has been suggested that host factors, including the presence or absence of specific immunoreactivity, may determine the success of parasite infections in various potential host species.

The immune response to invasive cyst infection is more pronounced but is often unsuccessful in eradicating the cyst in susceptible hosts. Infiltration with neutrophils and eosinophils is followed by local fibrosis, leading to cyst encapsulation and macrophage infiltration. Once the cyst is encapsulated, antigen release may be limited, leading to a reduction in the local inflammatory response. Specific antibody production remains detectable in the serum, however, and delayed-type hypersensitivity may be detected on skin testing. The immune response often increases later as the cyst begins to die and leak antigen or as it erodes into a body cavity, duct, or vessel, increasing local or systemic exposure to antigen. Experimentally, the anticyst immune response appears to limit dissemination of Echinococcus spp. after an initial infection. Anticyst immunity is also likely to contribute to the spontaneous clearance of H. nana infection in older children. There is evidence of increased amounts of IgG subclasses as well as proinflammatory cytokines within the cerebrospinal fluid (CSF) of patients having severe neurocysticercosis. It is unclear if this response contributes to the severity of the disease or is a consequence of severe infection; however, it does not effectively control the infection. Furthermore, symptomatic cysticercosis appears to be related to a depressed cellular immune response compared with the immune response of asymptomatic individuals.

Diphyllobothrium latum

D. latum, or fish tapeworm, is one of the pseudophyllidean cestodes transmitted via aquatic species. Human infection with D. latum is acquired by eating uncooked freshwater fish containing the parasite's plerocercoid cysts. Traditional modes of infection include consumption of dried or smoked fish, which may contain viable cysts if not further cooked, or tasting flavored freshwater fish (e.g., gefilte fish) before cooking. The enthusiasm for raw bar foods such as ceviche, sushi, and sashimi prepared from freshwater fish, especially salmon, has increased the transmission potential for D. latum in developed areas of North America. Areas of the world in which D. latum is highly endemic (>2% prevalence) include specific lake and delta areas of Siberia, Europe (especially Scandinavia and other Baltic countries), North America, Japan, and Chile. In 2006 there was an outbreak in Lake Geneva, Switzerland, caused by freshly caught raw perch served at a wedding. Plerocercoids were also found in 6% to 25% of fish caught in four Italian lakes. Endemicity in rural areas is favored by stable zoonotic transmission through alternative nonhuman definitive hosts including seals, cats, bears, minks, foxes, and wolves.

Human D. latum tapeworms are large, reaching up to 25 m (3000–4000 proglottids) in length. It takes 3 to 6 weeks after exposure for the tapeworm to mature. Once established, a D. latum parasite may survive 30 years or more. Multiple tapeworms in the same patient are common. Normally, infection is asymptomatic, but a proportion of infected individuals report nonspecific symptoms of weakness (66%), dizziness (53%), salt craving (62%), diarrhea (22%), and intermittent abdominal discomfort.

Prolonged (more than 3 or 4 years) or heavy D. latum infection may lead to megaloblastic anemia caused by vitamin B ₁₂ deficiency. The vitamin B ₁₂ deficiency is a consequence of two factors: parasite-mediated dissociation of the vitamin B ₁₂ intrinsic factor complex in the gut lumen (making vitamin B ₁₂ unavailable to the host) and heavy vitamin uptake and use by the parasite. Megaloblastic anemia may be worsened by concurrent folate deficiency, which also occurs as a consequence of D. latum infection. Vitamin B ₁₂ deficiency may be sufficiently severe to cause injury to the nervous system including peripheral neuropathy and severe combined degeneration of the central nervous system (CNS).

Tapeworm infection may first be suspected based on the patient's history or when contrast studies of the intestine show an intraluminal, ribbon-like filling defect. Definitive diagnosis of D. latum infection is made by detection of 45- × 65-mm operculated parasite eggs on stool examination ( Fig. 289.3A–B ). Recovery of proglottids (with a characteristic central uterus) also establishes the diagnosis.

Treatment is with a single course of niclosamide or praziquantel (see “ Therapy ”). Mild vitamin B ₁₂ deficiency is reversed by eradicating the tapeworm. Severe vitamin B ₁₂ deficiency should be treated with parenteral vitamin injections. If a patient presents with vitamin B ₁₂ deficiency and epidemiologic risk factors for fish tapeworm infection, one should maintain a high index of suspicion for possible infection.

Hymenolepis nana

H. nana, also known as dwarf tapeworm, is a cyclophyllidean tapeworm with embryonated eggs. It is probably the most prevalent tapeworm worldwide, and it is the only tapeworm that can be transmitted directly from human to human. Areas of endemicity (1%–30% prevalence) include Asia, southern and eastern Europe, Central and South America, and Africa. In North America, infection is most frequently found among institutionalized populations (up to 8% prevalence reported in the past) and among malnourished or immunocompromised patients.

Ingestion of parasite eggs on fecally contaminated food or fomites allows the initial infection. Once in the intestine, the eggs hatch to form oncospheres, which penetrate the mucosa to encyst as cysticercoid larvae. The larval cyst ruptures 4 or 5 days later into the lumen to form the relatively small, adult H. nana tapeworm (15–50 mm in length). Internal autoinfection may occur as parasite eggs are released from gravid proglottids in the ileum. In addition, poor sanitary practices promote external (fecal-oral) autoinfection as well as transmission to others sharing the same living quarters. Heavy infection is common among children and may be associated with abdominal cramps, anorexia, dizziness, and diarrhea. In areas of mass drug administration for other soil-transmitted helminth infections, H. nana has emerged as a prevalent pathogen because it does not respond to albendazole or mebendazole therapy given for intestinal nematodes. H. nana has been associated with anemia and weight loss among affected children.

H. nana infection is diagnosed by identifying the 30- × 47-µm parasite eggs (with their characteristic double membrane) in the stool ( Fig. 289.3C–D ). Treatment is with praziquantel or niclosamide (see “ Therapy ”). Developing H. nana cysticercoids are not as susceptible to drug therapy as adult tapeworms. Because these cysts can emerge several days later to form new tapeworms, effective therapy for H. nana requires either higher than usual doses of praziquantel to reach cysticidal levels or more prolonged therapy with niclosamide (to eliminate emerging tapeworms) for 5 to 7 days. Nitazoxanide has also been used to treat infection; it appears to be highly effective and has been used as an alternative therapy after treatment failures with niclosamide.

Taenia saginata

T. saginata, known as the beef tapeworm, is transmitted to humans in the form of infectious larval cysts found in the meat of cattle, which serve as the parasite's usual intermediate host. The T. saginata tapeworm is common in cattle-breeding areas of the world. Areas with the highest prevalence (up to 27%) are in central Asia, the Near East, and central and East Africa. Areas of lower prevalence (<1%) are found in Europe, Southeast Asia, Central America, and South America. Consumption of measly (i.e., cyst-infected) uncooked or undercooked beef is the usual means of transmission. Rare steak or kebabs and steak tartare are dishes typically associated with T. saginata infection. In the definitive human host, adult T. saginata tapeworms are long (10 m) and can contain more than 1000 proglottids, each capable of producing thousands of eggs. If, through poor sanitary practices, eggs released in the feces are allowed to reach grazing areas, cattle are subsequently infected with T. saginata cysticerci. Alternative intermediate hosts include llamas, buffalo, and giraffes. Humans are the only definitive host.

Symptoms are absent in most patients with T. saginata infection. A small number report mild abdominal cramps or malaise. The proglottids of T. saginata are motile and occasionally migrate out of the anus, to be found in the perineum or on clothing. The patient may report seeing moving segments in the feces or passing several feet of strobila at one time. These events are often psychologically distressing and are associated with significant anxiety-associated symptoms.

Specific diagnosis of T. saginata infection can be established by recovery of parasite proglottids. If only eggs are found in the stool, it is important to note that T. saginata eggs are morphologically indistinguishable from T. solium eggs ( Fig. 289.3E–F ). With T. solium tapeworms there is potential for autoinfection causing cysticercosis; therefore if any Taenia spp. eggs are detected, treatment should be given without delay for further speciation. Effective oral treatment for either T. saginata or T. solium is obtained with praziquantel or niclosamide (see “ Therapy ”).

Taenia solium

Humans can serve as either intermediate or definitive hosts for T. solium . Individuals who ingest T. solium eggs develop tissue infection with parasite cysts, a condition known as cysticercosis (see “ Cysticercosis ” for details of this illness). Patients who consume raw or undercooked pork containing infectious larval cysts (cysticerci) acquire the pork tapeworm—that is, the adult form of T. solium, which resides in the intestinal tract. These tapeworms develop to 2 to 8 m in length and may survive for 10 to 20 years. Some patients harbor both cysticerci and T. solium tapeworms, and it is possible for a tapeworm-carrying individual to develop cysticercosis by autoinfection. Areas in which T. solium infection is endemic include Mexico, Central America, South America, Africa, Southeast Asia, India, the Philippines, and southern Europe.

Infection with T. solium tapeworms is generally asymptomatic unless cysticercosis, caused by autoinfection with parasite eggs, supervenes. If tapeworm infection is diagnosed, one should also have a high index of suspicion for concomitant cysticercosis. The proglottids of T. solium are not motile (in contrast to those of T. saginata ) and do not migrate. Infection with Taenia spp. is readily diagnosed by detecting eggs during stool examination, but T. solium eggs are indistinguishable from T. saginata eggs (see Fig. 289.3E–F ). If a proglottid is recovered, the species can be identified based on the characteristic features of the uterine canals in the segment. Species identification is not required for therapy, which can be with either praziquantel or niclosamide.