Chapter 56: Cestodes

MORPHOLOGY

Like all helminths, tapeworms lack vascular and respiratory systems. In addition, they are devoid of both gut and body cavities. Nutrients are absorbed across their surface cuticle, and the internal organs are embedded in solid parenchyma. The adult is divided into three distinct parts: The “head” or scolex; a generative “neck”; and a long, segmented body called the strobila. The scolex typically measures less than 2 mm in diameter and is equipped with muscular sucking disks used to attach the worm to the intestinal mucosa of its host. (In one genus, Diphyllobothrium, the disks are replaced by two grooves called bothria.) As a further aid in attachment, the scolex of some species possesses a retractable protuberance, or rostellum, armed with a crown of chitinous hooks. Immediately posterior to the scolex is the neck from which individual segments, or proglottids, are generated one at a time to form the chain-like strobila. Each proglottid is a self-contained hermaphroditic reproductive unit joined to the remainder of the colony by a common cuticle, nerve trunks, and excretory canals. Its male and female gonads mature and self-fertilize as the segment is pushed farther and farther from the neck by the formation of new proglottids. When the segment reaches gravidity, it releases its eggs by rupturing, disintegrating, or passing them through its uterine pore.

TAENIA SAGINATA: PARASITOLOGY AND LIFE CYCLE

Taenia saginata inhabits the human jejunum, where it may live for up to 25 years and grow to a maximum length of 10 m. Its 1 mm scolex lacks hooklets but possesses the four sucking disks typical of most cestodes (Figure 56–1A). The creamy white strobila consists of 1000 to 2000 individual proglottids. The terminal segments are longer (20 mm) than they are wide (5 mm), and contain testes and a large uterus with 15 to 20 lateral branches; these characteristics are useful in differentiating them from those of the closely related pork tapeworm, Taenia solium (see later). When fully gravid, strings of six to nine terminal proglottids, each containing approximately 100 000 eggs, break free from the remainder of the strobila. These muscular segments may crawl unassisted through the anal canal or be passed intact with the stool. Proglottids reaching the soil may remain motile for a time, perhaps in order to move away from human feces and into fresh grass that will entice a cow during grazing. Eventually the proglottids disintegrate, releasing their distinctive ova. These eggs are 30 to 40 μm in diameter, spherical, and possess a thick, radially striated shell which appear very similar to those of T solium (Figure 56–1B). In appropriate environments, the embryo may survive in the egg for months. If ingested by cattle or certain other herbivores, the embryo is released, penetrates the intestinal wall, and is carried by the vascular system to the striated muscles of the tongue, diaphragm, and hindquarters. Here it transforms into a white, ovoid (5 by 10 mm) cysticercus (Cysticercus bovis). When present in large numbers, cysticerci impart a spotted or “measly” appearance to the flesh. Humans are infected when they ingest inadequately cooked meat containing these larval forms, which evaginate into scolices, attach to the jejunal epithelium, and begin to grow into a full-sized adult tapeworm, thus completing the life cycle.

BEEF TAPEWORM DISEASE

EPIDEMIOLOGY

In the United States, sanitary disposal of human feces and federal inspection of meat have nearly interrupted transmission of T saginata. At present, fewer than 1% of examined carcasses are infected. Nevertheless, bovine cysticercosis is still a significant problem in the southwestern area of the country, where cattle become infected in feedlots or while pastured on land irrigated with human sewage or worked by infected laborers who have insufficient access to sanitary facilities. Shipment of infected carcasses can result in human infection in other areas of the United States. In countries where sanitary facilities are less comprehensive and undercooked or raw beef is eaten, T saginata is highly prevalent. Examples include Kenya, Ethiopia, the Middle East, the former Yugoslavia, and parts of the former Soviet Union and South America.

BEEF TAPEWORM DISEASE: CLINICAL ASPECTS

MANIFESTATIONS

Most persons infected with beef tapeworm are asymptomatic and become aware of the infection only through the spontaneous passage of proglottids. The proglottids may be observed on the surface of the stool or appear in the underclothing or bedsheets of the alarmed host. Passage may occur irregularly and can be precipitated by excessive alcohol consumption. Some patients report epigastric discomfort, nausea, abdominal irritability, diarrhea, and weight loss. Occasionally, the proglottids may obstruct the appendix, biliary duct, or pancreatic duct.

DIAGNOSIS

The diagnosis of beef tapeworm disease is made by finding eggs or proglottids in the stool. Eggs may also be distributed on the perianal area secondary to rupture of proglottids during passage. The adhesive cellophane tape technique described for pinworm can be used to recover the worms from this area. With this procedure, 85% to 95% of infections are detected, in contrast to only 50% to 75% by stool examination. Because the eggs of T solium and T saginata are morphologically identical, it is necessary to examine a proglottid to identify the species correctly. As discussed below, the implications and management of these two infections may be substantially different.

TREATMENT AND PREVENTION

The drug of choice is praziquantel, which acts directly on the worm and is highly effective in single-dose oral preparations. To ensure cure, fecal specimens should be examined again approximately 3 months following treatment. Ultimately, control is best achieved through the sanitary disposal of human feces. Meat inspection is helpful; the cysticerci are readily visible. In areas where the infection is common, thorough cooking is the most practical method of control. Internal temperatures of 56°C or more for 5 minutes or longer destroy the cysticerci. Salting or freezing for 1 week at −15°C or below is also effective.

TAENIA SOLIUM: PARASITOLOGY AND LIFE CYCLE

Like the beef tapeworm, which it closely resembles, T solium inhabits the human jejunum, where it may survive for decades. It can be distinguished from its close relative only by careful scrutiny of the scolex and proglottids; T solium possesses a rostellum armed with a double row of hooklets (Figure 56–1B3). The strobila is generally smaller than that of T saginata, seldom exceeding 5 m in length or containing more than 1000 proglottids. Gravid segments measure 6 by 12 mm and thus appear less elongated than those of the bovine parasite (Figure 56–1B4). Typically, the uterus has only 8 to 12 lateral branches. Although the eggs appear morphologically identical to those of T saginata, they are infective only to swine and—perhaps reflecting a genetic proximity we might prefer to overlook—humans. Unlike T saginata, both pigs and people may become intermediate hosts when they ingest food contaminated with viable eggs (Figure 56–2). Humans with tapeworms may be autoinfected when gravid proglottids are carried backward into the stomach during the act of vomiting, initiating the release of the contained eggs. Autoinfection probably also results when eggs are transported from the perianal area to the mouth on contaminated fingers. The pork tapeworm life cycle is illustrated in Figure 56–2.

Regardless of the route of entry, an egg reaching the stomach of an appropriate intermediate host hatches, releasing an embryo called a “hexacanth,” because it has six hooklets. The embryo penetrates the intestinal wall and may be carried by the lymphohematogenous system to any tissue in the body. There it develops into a 1 cm, white, opalescent cysticercus over 3 to 4 months (Figure 56–3). The cysticercus may remain viable in pigs for up to 5 years, eventually infecting humans when they ingest undercooked “measly” flesh. In the human gut, the scolex everts, attaches to the mucosa, and develops into a new adult worm, thereby completing the cycle. When humans eat eggs, we serve as accidental, dead-end hosts, because the cysts will never be eaten by another person. However, these cysts may cause seizures if they form in the brain.

In summary, patients will acquire pork tapeworms if they consume undercooked pork; they will acquire cysticercosis if they consume tapeworm eggs from human feces.

PORK TAPEWORM DISEASE

EPIDEMIOLOGY

Although infected swine are still occasionally found in the United States, most human disease is diagnosed in immigrants from endemic areas. Although pork tapeworm disease is widely distributed throughout the world, it is particularly common in South and Southeast Asia, Africa, Latin America, and Eastern Europe.

PORK TAPEWORM DISEASE: CLINICAL ASPECTS

MANIFESTATIONS

The signs and symptoms of infection with the adult worm are mild and similar to those of T saginata taeniasis. However, clinical manifestations are totally different when humans serve as intermediate hosts. Cysticerci develop in the subcutaneous tissues, muscles, heart, lungs, liver, eye, and brain (Figure 56–4). As long as their number is small and the cysticerci remain viable, tissue reaction is moderate and the patient is typically asymptomatic. The death of the larvae, however, may lead to a marked inflammatory reaction, fever, muscle pains, and eosinophilia.

The most important and dramatic clinical presentation of lesions in the central nervous system (CNS) called neurocysticercosis. During the acute invasive stage, patients may experience fever, headache, and eosinophilia. In heavy infections, a meningoencephalitic syndrome with cerebrospinal fluid (CSF) eosinophilic pleocytosis may be present. Established cysts can be found in the cerebrum, ventricles, subarachnoid space, spinal cord, and eye. Cerebral cysts are usually small, often measuring 2 cm or less in diameter; racemose (clustered) lesions may be threefold larger. Parenchymal infections can induce focal neurologic abnormalities, personality changes, intellectual impairment and/or seizures; in many endemic areas, cysticercosis is the leading cause of epilepsy. Subarachnoid lesions and cysticerci located within the fourth ventricle may obstruct the flow of CSF, producing increased intracranial pressure with associated headache, vomiting, visual disturbances, or psychiatric abnormalities. Multiple lesions have a predilection for the basal cisterns. Spinal involvement produces cord compression or meningeal inflammation. Eye lesions incite pain and visual disturbances.

DIAGNOSIS

Infection with the adult worm is diagnosed as described for T saginata. Cysticercosis is suspected when an individual who has been in an endemic area presents with neurologic manifestations or subcutaneous nodules. Radiographs of the soft tissues may reveal dead, calcified cysticerci. Viable lesions may be detected as low-density masses by computed tomography (CT) or magnetic resonance imaging (MRI). Brain cysticerci typically are 5 to 10 mm in diameter (Figure 56–4). Subarachnoid lesions are often larger, may be lobulated, and are often “isodense,” making them difficult to identify radiographically. The lesions may resemble brain malignancy, which is managed differently, and thus it is important to confirm the diagnosis. This can be done by demonstrating the larva in a biopsy sample of a subcutaneous nodule or by detecting specific antibodies in the circulating blood. Serum and CSF enzyme immunoassays and western blot testing for specific anticysticercal antibodies have a sensitivity of 80% to 95%. The presence of IgG antibodies alone may reflect the presence of past or inactive disease.

TREATMENT AND PREVENTION

Infection with the adult worm is treated with praziquantel, as described for T saginata. Symptomatic neurocysticercosis requires a different approach. For patients who present with seizures, antiepileptic medications are the most important priority; treatment of brain parenchymal lesions can then be attempted with albendazole and corticosteroids (to help minimize the inflammatory response to dying cysticerci). However, seizure control—not antiparasitic medication—is the first priority. Mechanical blockage of the brain’s ventricles is another feared complication. Intraventricular, subarachnoid, and eye lesions appear relatively refractory to chemotherapy; surgery, CSF shunts, and corticosteroids may help ameliorate symptoms. Tapeworm acquisition can be prevented by adequately cooking pork before ingestion. Egg ingestion can be prevented by proper hand hygiene among food service workers after using the toilet.

DIPHYLLOBOTHRIUM LATUM: PARASITOLOGY AND LIFE CYCLE

The adult D latum attaches to the human ileal mucosa with the aid of two sucking grooves (bothria) located in an elongated fusiform scolex (Figure 56–5). In life span and overall length, it resembles the Taenia species discussed previously. The 3000 to 4000 proglottids, however, are uniformly wider than they are long, accounting for this cestode’s species designation as well as one of its common names, the “broad tapeworm.” The gravid segments contain a centrally positioned, rosette-shaped uterus unique among the tapeworms of humans. Over 1 million oval (55 by 75 μm) operculated eggs are released daily into the stool (Figure 56–5).

On reaching fresh water the eggs hatch, releasing ciliated, free-swimming larvae called coracidia. If ingested within a few days by small freshwater crustaceans of the genera Cyclops or Diaptomus, they develop into procercoid larvae. When the parasitized crustacean is then ingested by a freshwater or anadromous marine fish, the larvae migrate into the musculature of the fish and develop into infectious plerocercoid larvae. Humans are infected when they eat improperly prepared freshwater fish containing such forms. The life cycle is illustrated in Figure 56–6.

FISH TAPEWORM DISEASE

EPIDEMIOLOGY

Fish tapeworms are found wherever raw, pickled, or undercooked freshwater fish from fecally contaminated lakes and streams are eaten by humans. Other fish-eating mammals like cats, dogs, and bears may serve as reservoir hosts. Human infections have been described in the Baltic and Scandinavian countries, Russia, Switzerland, Italy, Japan, China, the South Pacific, Chile, and Argentina. The worm, possibly brought to North America by Scandinavian immigrants, is now found in Alaska, Canada, the midwestern states, California, and Florida. In the Pacific Northwest and Pacific Rim, a closely related species Diphyllobothrium nihonkaiense seems comparatively hardy in cold conditions and is able to form infectious plerocercoid larvae in anadromous salmon. Human cases have been traced to the ingestion of fish freshly taken from Alaskan waters. The increasing popularity of raw fish dishes, such as Japanese sushi and sashimi, may lead to increased prevalence of this disease in the United States—although freezing the fish before consumption is usually fatal to the cysts. Among native Americans, infection has been acquired by eating salted fish. Even when fish is appropriately cooked, individuals may become infected by sampling the flesh during the process of preparation.

FISH TAPEWORM DISEASE: CLINICAL ASPECTS

MANIFESTATIONS

Most infected patients are asymptomatic. On occasion, however, they may complain of epigastric pain, abdominal cramping, vomiting, and weight loss. Moreover, the presence of several adult worms within the gut has been known to precipitate intestinal or biliary obstruction. Forty percent of fish tapeworm carriers demonstrate low serum levels of vitamin B₁₂, apparently because of the competition between the host and the worm for this ingested nutrient. Studies have shown that a worm located high in the jejunum may take up 80% to 100% of vitamin B₁₂ given by mouth. Approximately 0.1% to 2% of patients develop macrocytic anemia. They tend to be elderly, to have impaired production of intrinsic factor, and to have worms located high in the jejunum. In many, folate absorption is also diminished. Lysolecithin, a tapeworm product, may also contribute to anemia. Neurologic manifestations of vitamin B₁₂ deficiency may occur, sometimes in the absence of anemia. They include numbness, paresthesias, loss of vibration sense, and, rarely, optic atrophy with central scotoma.

DIAGNOSIS

The diagnosis should be suspected among patients with a compatible dietary history, ill-defined GI symptoms, or B₁₂ deficiency. It is confirmed by finding eggs in the stool. Because D latum produces large numbers of ova, identification is usually accomplished without the need for concentration techniques.

TREATMENT AND PREVENTION

Treatment is the same as described for T saginata tapeworm infections, using praziquantel. When anemia or neurologic manifestations are present, parenteral administration of vitamin B₁₂ is also indicated. Personal protection can be accomplished by thorough cooking of all salmon and freshwater fish. Devotees of raw fish may choose to freeze their favorite dish at −10°C for 48 hours before serving, as this is also effective in killing the plerocercoids. Ultimately, control of diphyllobothriasis is accomplished by prohibiting the discharge of untreated sewage into lakes and streams, although animal reservoir hosts are not addressed via this technique.

Echinococcosis, or “hydatid disease,” is a tissue infection of humans caused by larvae of Echinococcus granulosus and E multilocularis. The former is a more common cause of human disease.

Echinococcus granulosus

PARASITOLOGY AND LIFE CYCLE

The adult E granulosus inhabits the small bowel of dogs, wolves, and other canines, where it survives for a scant 12 months. The scolex possesses four sucking disks and a double row of hooklets. The entire strobila, however, measures only 5 mm in length, and contains but three proglottids: One immature, one mature, and one gravid. The latter segment splits open either before or after passage in the stool, releasing eggs that appear identical to those of T saginata and T solium. A number of mammals may serve as intermediates, including sheep, goats, camels, deer, caribou, moose, and—most importantly—humans. When one of these hosts ingests eggs, they hatch, releasing embryos that penetrate the intestinal mucosa and are then carried via the portal blood to the liver. There, many are trapped in the hepatic sinusoids. The rest traverse the liver and are carried to the lung, where they may lodge. A few pass through the pulmonary capillaries, enter the systemic circulation, and are carried to the brain, heart, bones, kidneys, and other organs. Many of the larvae are phagocytosed and destroyed by host immune cells. The survivors form a cyst wall composed of an external laminated cuticle and an internal germinal membrane. The cyst fills with fluid and slowly expands, reaching a diameter of 1 cm over the next 5 to 6 months (Figure 56–7). However, they may grow substantially larger in subsequent months and years, in some cases reaching diameters greater than 10 cm. In time, secondary “brood capsules” arise from the germinal layer and form within the original hydatid, or break through the cyst surface to form new “daughter cysts.” Within these brood capsules and daughter cysts, new protoscolices develop from the germinal lining. Degenerated protoscolices and germinal membranes fall to the bottom of the cyst to form hydatid “sand.” When hydatid-containing tissues of the intermediate host are ingested by a canine, scolices are released in the intestine where they develop into adult worms. The life cycle is illustrated in Figure 56–8.

ECHINOCOCCOSIS

EPIDEMIOLOGY

There are two major epidemiologic forms of E granulosus-induced echinococcosis: Pastoral and sylvatic. The more common pastoral form has its highest incidence in Australia, New Zealand, South and East Africa, the Middle East, Central Europe, and South America, where domestic herbivores such as sheep, cattle, and camels are raised by people in close contact with domestic dogs. Although approximately 200 human cases are reported each year in the United States, most were acquired elsewhere. Indigenous cases have been reported, however, particularly among Basque sheep farmers in western states and Native Americans in the southwest. Animal husbandry practices that permit dogs to feed on the raw viscera of slaughtered sheep perpetuate cycle. Transmission also depends on suboptimal hand hygiene, in that shepherds become infected while handling their dogs: Eggs are transferred from dog feces to their fur, where they are relocated onto their masters’ hands and later ingested. Sylvatic echinococcosis, in contrast, is found principally in Alaska and western Canada, where wolves act as the definitive hosts and moose or caribou are the intermediates. In two counties in California, a second sylvatic cycle involving deer and coyotes has been described. When hunters kill these wild deer and feed their offal to accompanying dogs, a pastoral cycle may be established.

ECHINOCOCCOSIS: CLINICAL ASPECTS

MANIFESTATIONS

The enlarging E granulosus cysts produce tissue damage by mechanical means. The clinical presentation depends on their number, location, and rate of growth. Typically, a latent period of 5 to 20 years occurs between acquisition of infection and subsequent diagnosis. Intervals as long as 75 years have been reported.

The majority of cysts are found in the liver, and/or in the lung. One-fifth of all patients show involvement of multiple sites. Many patients are asymptomatic when the lesion is discovered on routine imaging or physical examination. Occasionally, the patient may present with hemoptysis, pain in the right upper quadrant of the abdomen, or a tender hepatic mass. Significant morbidity is uncommon, and death rare. However, hydatid cysts may reach enormous size (Figure 56–7B). They may eventually rupture, inducing fever, pruritus, urticaria, and—at times—anaphylactic shock. Germinal tissue or brood capsules may also spread to other areas, leading to dissemination of the infection. Rupture of pulmonary lesions also induces cough, chest pain, and hemoptysis. Liver cysts may break through the diaphragm or rupture into the bile duct or peritoneal cavity. Most patients who develop symptoms, however, present with a tender, palpable hepatic mass. Intrabiliary extrusion of calcified cysts may mimic the signs of acute cholecystitis; complete obstruction results in jaundice. Bone cysts produce pathologic fractures. Lesions in the CNS may manifest with blindness or seizures. Cardiac lesions have been associated with conduction disturbances, ventricular rupture, and embolic metastases. It has been suggested that circulating antigen–antibody complexes may deposit in the kidney, initiating membranous glomerulonephritis.

DIAGNOSIS

In E granulosus-infected patients, chest X-rays may demonstrate pulmonary lesions as slightly irregular, round masses of uniform density, often devoid of calcification. In contrast, more than one-half of hepatic lesions display a smooth, calcific rim. CT, ultrasonography, and MRI may reveal either a simple fluid-filled cyst or daughter cysts with hydatid sand. Endoscopic retrograde cholangiography has been valuable for determining cyst location and possible communication with the biliary tree. Because of the potential for an allergic reaction or spread of infection, diagnostic aspiration may be contraindicated. Nevertheless, in select cases, ultrasonically guided percutaneous drainage, followed by the introduction of hypertonic saline to kill protoscolices and germinal layer, has proved safe and useful both diagnostically and therapeutically (see PAIR later). In patients with ruptured pulmonary cysts, scolices may be demonstrated in the sputum.

In some cases, confirmation of the diagnosis before drainage requires serologic testing. Unfortunately, current options are not totally satisfactory. Indirect hemagglutination and latex agglutination tests are positive in 90% of patients with hepatic lesions and 60% of those with pulmonary hydatid cysts. Polymerase chain reaction assay has been shown to be capable of detecting picogram quantities of Echinococcus genomic DNA in fine-needle biopsy material from patients with suspected echinococcosis.

TREATMENT AND PREVENTION

For years, the only definitive therapy available was surgical extirpation. Patients with pulmonary hydatid cysts of the sylvatic type and small calcified hepatic lesions underwent surgery only when they became symptomatic or the cysts increased dramatically in size over time. However, for uncomplicated lesions, Puncture, Aspiration, Infusion of scolicide, and Reaspiration (PAIR) can be used in lieu of surgery. The scolicide of choice is probably hypertonic saline, although other chemicals have been used. If performed properly, this technique is safer and better tolerated than open surgery. Presently, it is recommended that high-dose albendazole be administered before and for several weeks (or years in the case of E multilocularis infection) after surgery and/or aspiration. Infected dogs should be dewormed, and infected carcasses and offal burned or buried. Hands should be carefully washed after contact with potentially infected dogs.

Echinococcus multilocularis

Echinococcus multilocularis is found primarily in subarctic and arctic regions in North America, Europe, and Asia. The adult worms are found in the gut of foxes and, to a lesser extent, coyotes. Their larval forms find harborage in the tissues of mice and voles, the rodent prey of canines. Domestic dogs may acquire adult tapeworms by killing and ingesting these larva-infected sylvatic rodents. Humans are infected with larval forms through the ingestion of eggs passed in the feces of their domestic dogs or ingestion of egg-contaminated vegetation. Unlike the larval forms of E granulosus, those of E multilocularis bud externally, producing proliferative, multilocular cysts that slowly but progressively invade and destroy the affected organs and adjacent tissues.

The clinical course in humans is characterized by epigastric pain, obstructive jaundice, and, less frequently, metastasis to the lung and brain, thus closely mimicking liver cancer. As with E granulosus, medical treatment of E multilocularis often fails to achieve cure. Patients with multilocular infection may require surgical management. The prognosis is grim if not diagnosed early.

Like Echinococcus species, and in contrast to the cow, pig, and fish tapeworms, the adult Hymenolepis nana worm is very small, perhaps 4 cm in length. Rodents are the most common definitive hosts, but humans may become infected as well. In fact, the so-called “dwarf tapeworm” is the only tapeworm that can be transmitted directly from human to human. Eggs are ingested via the fecal–oral route. They then release embryos that penetrate the intestinal wall. The resulting cysts mature in the intestinal wall, then reenter the gut lumen to develop into adult worms again. Endemic areas include parts of Asia, Europe, Central and South America, and Africa. Occasionally, it is found in institutionalized persons in North America. Most persons are asymptomatic, but heavy worm burdens may be associated with diarrhea, abdominal cramping, and anorexia. Finding characteristic eggs in the stool makes the diagnosis. Treatment is similar to that for other tapeworms, but may need to be prolonged to fully eradicate cysts in the intestinal wall.