Human tapeworms, Taenia spp.

Taenia spp. (tapeworms) taxonomy and origin

Taenia solium lineage:

cellular organisms - Eukaryota - Fungi/Metazoa group - Metazoa - Eumetazoa - Bilateria - Acoelomata - Platyhelminthes - Cestoda - Eucestoda - Cyclophyllidea - Taeniidae - Taenia -

Human tapeworms

Taenia solium - pork tapeworm
Taenia saginata - beef tapeworm
Taenia asiatica - Asian tapeworm

Zoonotic tapeworms

Taenia crassiceps
Taenia ovis
Taenia taeniaeformis
Taenia hydatigena
Taenia multiceps
Taenia serialis
Taenia brauni

Taenid tapeworms are helminth endoparasites belonging to order Platyhelminthes (flatworms).

The Taenids are unique in having mammals as both definitive (harboring adult parasites) and intermediate (harboring larval parasites) hosts.
Their transmission and life cycles are linked to specific predator–prey assemblages: a carnivorous or omnivorous definitive host gets infected by eating its prey, an intermediate host. Switching among carnivorous definitive hosts (e.g., among canids, felids, hyaenids and humans) that have historically exploited common prey resources played a crucial role in Taenid speciation (formation of new biological species).

To answer the question how species of human-specific taenids arose, it was proposed initially that in early times of animal husbandry (not more than 10,000 years ago), tapeworms circulating between dogs and domesticated ruminants were the source of first Taenia that colonized humans. More recent phylogenetic studies based on molecular data had estimated age for divergence of human-specific T. saginata and T. asiatica at 0.78–1.71 million years ago which suggest that the parasites adapted to Homo sapiens much earlier than domestication started. Shift of human diet from herbivory to omnivory and, later, to facultative carnivory 2.0–2.5 million ago was necessary for the adaptation of the tapeworms to human host.

Maintenance of T. solium within populations of Homo may have further been facilitated by cannibalism in a unique "human–human cycle".

T. asiatica as a separate species was discovered relatively recently. It had been mistaken for Taenia saginata Goeze (1782) for more than 200 years and later was classified as subspecies of T. saginata. However, extensive epidemiological, molecular, comparative morphology and phylogenetic analyses have indicated the independent and specific status of T. asiatica (Eom & Rim 1993).

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Brief facts

• Species of Taenia were among the earliest recognized helminths in humans, with written records of their occurrence extending into antiquity.
• Many tapeworms have indirect life cycle that requires an intermediate host for larval stage of the parasite.
• Usually the larvae of the tapeworm develop in flesh of prey animals (intermediate hosts), where asexual reproduction of the parasite can occur, and sexual egg-laying adult develops in intestinal tract of the predator.
• Larval infection is called cysticercosis (Taenia solium, T. saginata, T. asiatica, T. crassiceps, T. ovis, T. taeniaeformis, and T. hydatigena) or coenurosis (T. multiceps, T. serialis, T. brauni). Disease that is caused by adult worms is called taenosis.
• There are three species of taenids that use humans as definitive hosts: Taenia solium, T. saginata, an T. asiatica. In addition, Taenia solium can also use humans as intermediate hosts causing cysticercosis. This ability makes this parasite especially important. Other species of taenids circulate in wild animals and infect humans only occasionally causing cysticercoses/coenuroses as well as taenoses.

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Developmental stages of Taenia spp. (Taenia solium, Taenia saginata, Taenia asiatica) and associated diseases.

Life cycles of all taenids are very similar. T. solium is distinguished by its ability to use humans not only as definitive hosts but also as intermediate hosts. Because of this, the species is most important within this group of parasites. There is currently no evidence that cysticerci of either T. saginata or T. asiatica can develop in humans.

• egg The eggs and distal gravid proglottids (section of worm's body full of infective eggs) are released in feces and can contaminate hands, water and food. Each egg contains an an oncosphere (embryo). Egg size: 30 - 40 µm. Each egg has hooklets and a striated outer shell. The eggs of different species are very difficult to differentiate. Eggs that are highly resistant to ambient environmental conditions, remaining viable for up to 8 months in warm and humid climates.
• larva (metacestode) The oncospheres released from eggs by the action of stomach trypsin cross the bowel wall, enter the bloodstream, and are carried to the tissues. At small terminal vessels, they establish and encyst as cysticerci, reaching their final size (0.5-2 cm) in 2–3 months. Cysticercus is a tapeworm larva that consists of fluid-filled vesicle, which contains single protoscolex as opposed to coenurus - a vesicle that contains multiple inverted protoscolices, attached to the internal membrane of the cyst. Daughter cysts may be seen inside some coenuri. Coenuri are characteristic to some zoonotic tapeworms (see below).
  • Porcine cysticercosis
    (T. solium) Cysticerci of T. solium establish themselves in the muscles (including cardiac and tongue) and central nervous system (spinal cord and brain). Most pigs are killed before the age of 9 months, which is too short period for detectable illness to develop even in case of massive infection. Commonly practiced way to diagnose the infection in pigs is tongue examination: visual inspection and palpation for cysts is easy and accurate when performed by a trained individual. Meat inspection and immunodiagnosis are also very useful ante-mortem strategies.
  • Human cysticercosis
    (T. solium) Human cytocercosis has same mechanism as the porcine cytocercosis outlined above except that infected people usually live long enough to develop symptoms. Cysts are uniformly rounded or oval vesicles, varying in size from a few millimetres to 1–3 cm (in rare cases a growing cyst reaches several centimetres in diameter). Vesicles vary in contents according to their evolutionary stage. Viable cysts have a translucent membrane through which the scolex is visible as a small 2–3 mm nodule. When the cyst starts to degenerate, the vesicular fluid becomes opaque and dense, and the edges of the cyst become irregular and shrink. After calcification is complete, the cyst becomes round, whitish nodule. Cysticercosis become symptomatic only when cysts are dying or become large enough to interfere with vital organs. The incubation period for cysticercosis can last from 10 days to 10 years.

    Neurocysticercosis (NCC)

    NCC is currently considered the most common parasitic disease of the central nervous system especially in endemic regions of Latin America, India, Asia, Eastern Europe and Africa. In NCC the cysts can be located about anywhere in the central nervous system (brain and spinal cord). Epileptic seizures are the most common presentation of neurocysticercosis and generally represent the primary or sole manifestation of the disease. Seizures occur in 50–80% of patients with parenchymal brain cysts or calcifications. Occasionally, a cyst grows larger than the usual 1–2 cm and acts in the same way as a tumoral mass (giant cyst). The racemose form is a large translucent vesicle, frequently lobulated, without a scolex, which develops in the basis of the brain or in the ventricles. The racemose form is associated with high mortality.

    Extraneural cysticercosis

    Outside the central nervous system, cysticercosis causes no major symptoms. Subcutaneous cysticercosis presents as small, movable, painless nodules that are most commonly noticed in the arms or chest. After a few months or even years, the nodules become swollen, tender, and inflamed, and then they gradually disappear.

    Ophthalmic cysticercosis

    T. solium is the most common intraorbital parasite. Intraocular cysts are most frequently found floating freely in the eye volume. Visual disturbances and even blindness are related to the degree of damage to retinal tissue or the development of chronic uveitis.
  • Bovine cysticercosis
    (T. saginata) Bovine cysticercosis is the source of substantial production losses, condemnation and destruction of infected cattle. Substantial economic impacts stem from increasing labor costs of handling infected carcasses and processes that are required to render cysticerci non-viable.
  • Porcine cysticercosis
    (T. asiatica) Oncospheres of T. asiatica exhibit viscero-tropism rather than musculo-tropism. Metacestodes reside in visceral organs such as the liver, spleen, omentum, and lungs, but not in the muscles.
• adult Association between cysticercosis and taenosis, which separately were known for ages, was found only in 1855 by Kuchenmaister. He fed condemned prisoners with cysticercosis-infected pork and recovered young tapeworms at autopsy.

  Transmission

  Taeniasis occurs after consumption of undercooked animal product infected with cysticerci: meat in case of T. solium and T. saginata and liver or other internal organs in case of T. asiatica.

  Growth and proliferation

  Soon after ingestion larvae reach small intestine where they evaginate and release the head (scolex), which attaches to the mucosa. From proliferating cells in the neck the scolex begins forming segments (proglottids) in the process that is known as strobilation. Hermaphroditic proglottids undergo continuous differentiation to eventually form gravid proglottids full of infective eggs. Tapeworms take up most of their nutrients from the host intestinal submucosa and detachment of the scolex from the site causes death of the tapeworm and its elimination. Attached intact scolex stripped of all its proglodits can regenerate. The outstanding feature of tapeworms is the syncytial nature of their tissue (cells are not completely separated exhibiting a cytoplasmic continuity between them). One of the many controversial issues about human tapeworm physiology is how the distal end of the strobila, which may be several meters away from the scolex, acquires nutrients. The distribution of cytoplasmic glycogen in experimental strobilae, suggests that the young proglottids may have abundant stores of glycogen, which become depleted as they are maturing. Adult tapeworms can grow up to 20 meters long, usually they reach 2-7 meters.

  Duration and symptomps

  Infections in humans may be of long duration, perhaps exceeding 20–25 years, in the absence of treatment. Clinical signs are limited, but may include nausea, dizziness, altered appetite, headache and other manifestations. Often infection is revealed by the spontaneous release of gravid proglottids. Toxic effects from parasite metabolites have also been reported. Most, carriers of T. solium will neither look for medical care nor notice the tapeworm segments in their stools. Conversely, most patients infected with T. saginata notice passage of proglottids, which are motile, more numerous, and larger than those of T. solium.

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Life cycle diagram of human tapeworms

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Pathways of animal cystisercosis

• direct transmission through fecal contamination from agricultural workers
• application of untreated human sewage sludge onto pastures and other areas where animals are allowed to roam
• indirect contamination of food products or water for cattle
• dissemination of parasite eggs by birds from sewage sources to feed bins, silage and cattle pens

Human hosts may release several segments daily, each containing thousands of eggs, and a single infected agricultural worker can be responsible for epizootic outbreaks in cattle or swine. Notably, eggs may remain infective in the environment for several months under suitable conditions.

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Eradication and control

Although all tapeworms represent a considerable animal and human health burden, T. solium remains as a primary target for eradication world-wide because of its ability to cause cysticercosis in humans. Autoinfection (when individual parasitized by adult worm ingests eggs expelled from its own body and becomes ill from cysticercosis) is considered a common occurence. The following characteristics of human-specific tapeworms make them vulnerable to eradication:

• the life cycle requires humans as its definitive host
• tapeworm infection in humans is the only source of infection for pigs and cattle, the natural intermediate hosts
• domestic pigs and cattle, the intermediate hosts, can be managed
• no significant wildlife reservoir exists
• practical intervention is available in the form of chemotherapy for human taeniosis and porcine cysticercosis with safe and effective drugs

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Desinfection

• Cysts die if meat is kept at 4 °C for more than 1 month, or frozen at − 20 °C for one to 3 days (T. solium) and at –10 °C for 10 days (T. saginata).
• Cooking meat to 56°C throughout for 30 min is sufficient to kill infective cysts (T. solium, T. saginata).
• T. solium and T. saginata are inactivated by 1% sodium hypochlorite or 2% glutaraldehyde.

Note: Undercooked, smoked or pickled meat can be infective.

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Brief comparison of human tapeworms

Definitive host	human	human	human
Characteristics	T. solium	T. asiatica	T. saginata
Intermidiate host	pig, human	pig	cattle
Larvae location	muscle, fat, brain	viscera, liver, spleen, lung and other internal organs	muscles including heart (one of easier diagnosed site), tongue
Adult worm scolex	double-crown of hooklets present, rostellum present	hooklets absent, rostellum with 4 suckers present	hooklets absent, rostellum absent, 4 suckers with small apical depression
Geographic distribution	world-wide with "hot spots" in Mexico and several countries in Central America, South Asia, and sub--Saharan Africa	Southeast Asia - Korea, Taiwan, Indonesia, Vietnam, China	world-wide including Europe, Africa, Middle East, and Asia; most highly endemic Taenia in United States

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Treatment

Human cysticercosis

Because extraneural cyctocercosis is usually benign, in majority of cases no treatment is necessary. However, because a proportion of people with cysticercosis may also be T. solium tapeworm carriers it may be unavoidable. Neurocysticercosis is associated with substantial morbidity and mortality and often requires treatment in order to alleviate symptoms and improve quality of life of infected people. The management of NCC may involve:

• Antiparasitic drugs. Antiparasitic treatment may be unnecessary or even contraindicated in some NCC patients (for example, in case of ocular or spinal cysts) while in others, it may be beneficial and even lifesaving. Between available antiparasitic drugs, niclosamide and praziquantel, niclosamide is the drug of choice because it is not absorbed from the intestines. With praziquantel there is a small risk that asymptomatic viable brain cysts are affected by the drug in serum, causing neurological symptoms such as headache and seizures.
• Steroids are usually administered in conjunction with antiparasitic therapy to suppress inflammation caused by disintegrating cysts.
• Antiepileptic drugs are the principal therapy for seizures associated with NCC, which may eventually be lessened or even dissapear with time. The presence of calcifications in the brain is a known risk factor for seizure relapse and the proportion of calcifying cysts may be higher in cysticercosis patients treated with antiparasitics.
• Surgery is performed when cysts can be safely removed. Surgery is usually required for treating hydrocephalus caused by NCC and is also appropriate for removal of ventricular, spinal or ophthalmic cysticerci.

Human taenasis

Both niclosamide (2 g orally in a single dose) and praziquantel (5 mg/kg orally in a single dose) are effective against the adult tapeworm. Praziquantel may reach serum levels high enough to affect brain cysts if the tapeworm carrier also has NCC, causing seizures or severe headaches. An elctrolyte-polyethylenglycol salt (EPS) purge is usually indicated short after the chemotherapy to expel the worm and avoid the potential risk of having proglottids or eggs returned to the stomach and digested, leading to internal autoinfection. It also greatly improves the recovery of tapeworm scolices and gravid proglottids which indicates cure as well as provides parasite material for species identification of the infecting worm.

Porcine cysticercosis

A veterinary benzimidazole and oxfendazole, is more than 95% effective in killing the cysts in the pig when given in a single dose of 30 mg/kg. Infested meat in oxfendazole-treated pigs needs at least eight weeks for all the cysts to degenerate and up to 12 weeks to achieve a clear, acceptable appearance of the pork for human consumption.

Bovine cysticercosis

Oxfendazole was developed for use as an anthelmintic for ruminants and is administered to cattle at an oral dose of 4.5 mg/kg.

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Other tapeworms that can affect humans

In humans domestic cats and dogs are potential sources of zoonotic cystocerosis and coenurosis infections and undercooked game meat can be source of zoonotic taenosis.

Species	Primary intermediate hosts/Alternative	Primary definitive host/Alternative	Type of larval infection	Larval tissue distribution	Geographic distribution
T. crassiceps	wild rodents / cats, humans	foxes/canids (wolves, coyotes, dogs)	cysticercus (can multiply by asexual budding)	subcutaneous tissues, peritonealor pleural cavities	Canada, northern United States
T. ovis	dogs, wild carnivores / rare in cats	sheep, goat	cysticercus	muscles	world-wide
T. taeniaeformis	rodents / very rare in humans	felids and canids	cysticercus	liver, spleen	world-wide
T. hydatigena	sheep, goats, cattle, pigs, reindeer / rare in rabbits, rodents, humans	dogs, wolves, coyotes, lynxes / rare in cats	cysticercus	liver, abdominal cavity attached to omentum and mesentery	world-wide
T. multiceps	sheep, goats, cattle / human	dogs, wolves, foxes, jackals	coenurus (2 - 6 cm in diameter)	muscles, brain, spinal cord, eye	some parts of Americas, Europe and Africa
T. serialis	hares, rabbits / squirrels, other rodents, cats, human	canids including dogs, coyotes, etc.	coenurus (up to 5 cm in diameter)	subcutaneous tissues, muscles, retroperitoneally	North America, Europe, Africa
T. brauni	rodents / human	canids	coenurus	subcutaneous tissues, eye	Africa

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References

• Willms K. Morphology and biochemistry of the pork tapeworm, Taenia solium. Curr Top Med Chem. 2008
• Haag KL, Gottstein B, Ayala FJ. Taeniid history, natural selection and antigenic diversity: evolutionary theory meets helminthology. Trends Parasitol. 2008 Feb.
• García HH et al. Strategies for the elimination of taeniasis/cysticercosis. J Neurol Sci. 2007 Nov 15.
• Willingham AL 3rd, Engels D. Control of Taenia solium cysticercosis/taeniosis. Adv Parasitol. 2006;61:509-66.
• Flisser A, Rodríguez-Canul R, Willingham AL 3rd. Control of the taeniosis/cysticercosis complex: future developments. Vet Parasitol. 2006 Jul 31.
• Eom KS. What is Asian Taenia? Parasitol Int. 2006;55 Suppl:S137-41. Epub 2006 Jan 4.
• Hoberg EP. Phylogeny of Taenia: Species definitions and origins of human parasites. Parasitol Int. 2006;55 Suppl:S23-30.
• Avila G et al. Laboratory animal models for human Taenia solium. Parasitol Int. 2006;55 Suppl:S99-S103.
• Flisser A. Where are the tapeworms? Parasitol Int. 2006;55 Suppl:S117-20. Epub 2005 Dec 6.
• Garcia HH et al. Diagnosis, treatment and control of Taenia solium cysticercosis. Curr Opin Infect Dis. 2003 Oct.
• García HH at al. Taenia solium cysticercosis. Lancet. 2003 Aug 16;362(9383):547-56.
• Hoberg EP. Taenia tapeworms: their biology, evolution and socioeconomic significance. Microbes Infect. 2002 Jul;4(8):859-66.

Websites

• Taenia infections. Institute for International Cooperation in Animal Biologics. 2005 (.pdf)
• Practical parasitology: Taenia Species

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