Parasites and Pestilence
(Institute of Tropical Medicine Antwerp)
Linguatulosis is a rare parasitic disease caused by parasites of the genus Linguatula, which are also known as “tongue worms” because of the worm’s generalized tongue shape. Linguatula serrata is the most common agent, and one of the few species of the Pentastomida phylum that infects humans. Linguatulosis is also referred to Marrara Syndrome in Sudan because of the traditional “marrara” dish that consists of raw sheep or goat liver that is commonly associated with the disease (John and Petri). In the Middle East, the disease is termed Halzoun Syndrome, after the traditional dish of kibbe (raw lamb or beef) that may result in the ingestion of infected lymph nodes (Mehlhorn). Epidemiological studies have shown Linguatula serrata to be found worldwide. Human infections have been reported from Africa, Europe, Asia, and the Americas, and they are common in Malaysia and Central Africa (John and Petri).
Pentastomiasis was first described as an animal infection in 1787 by a French veterinary surgeon by the name of Chabert, who found Linguatula serrata in the nasal cavities of several dogs. It was not described as a human infection until 1847 by a man names Pruner in Cairo, Egypt. Soon thereafter, the disease received much attention from pathologist Sambon and from famous zoologist and parasitologist Rudolf Leuckart (Cannon).
Though most cases of Linguatulosis are asymptomatic, clinical presentation in humans can take two forms. The first is the more common visceral infection. This form is usually asymptomatic but may present with eye lesions due to ingestion of ova. When the embryo reaches the intestine, it develops into a primary larval form that crosses the intestinal wall and migrates to different organs like the liver, lungs, mesenteric lymph nodes, and sometimes brain and prostate gland. At these sites, the larvae become encysted and develop further until they mature into nymphs. Nymphs rarely produce clinical symptoms. When nymphs die after a year or more, they may calcify and are often discovered only during autopsy or radiological exams (Lazo et al). The second is the nasopharyngeal infection, which is termed Marrara or Halzoun Syndrome (GIDEON), as described above. The migration of ingested larvae from raw sheep liver or lymph nodes causes symptoms of irritated and sore throat, edema, and congestion that may extend to the larynx (Lazo et al). As of 1999, ocular infection had only been described in Israel, Ecuador, and the United States (GIDEON).
(Lazo et al)
Infection occurs through consumption of Linguatula serrata eggs, which may be present in raw vegetables or contaminated water, uncooked sheep (particularly the liver and lymph nodes) or snake meat (John and Petri). As explained above, ingested eggs hatch in the intestine and larvae then penetrate the intestinal wall and migrate to various sites where they develop into nymphs. A definitive incubation period of Linguatulosis is unknown (GIDEON). Some researchers suggest anywhere from seven days to months (Mehlhorn). It has also been suggested that nymphs may persist in various sites of the human host for a year or more (Lazo et al).
Pentastomes live mainly in the respiratory passages of carnivorous reptiles, birds, and mammals, which serve as definitive hosts. Encapsulated eggs are passed in the sputum or feces of an infected definitive host, and are then ingested by an intermediate host in which larval development occurs. Intermediate hosts include fish, rodents, rabbits, or small ungulates (John and Petri). A recently published study reports that the prevalence of Linguatula serrata infection among ruminants in South India is higher than previous reports from the region. The article points to the strong focus of infection in herbivorous domesticated mammals of South India, which include goats, cattle and buffaloes, each revealing an infection prevalence of 21, 19, and 8%, respectively (Ravindram et al). Humans may act as intermediate or accidental definitive host of the linguatula parasite (Lazo et al). There is no vector.
As mentioned above, Pentastomes are often referred to as “tongue worms” because of the tongue-like structure of the Linguatula genus. However, some Pentastomes resemble arthropods, a close relative, and are most are cylindrical with annelid (segmented worm)-like features. The name Pentastoma comes from what appears to be five ventral openings or mouths, which in actuality are one mouth and four hooks (John and Petri). (See below.) Nymphs of the third instar larval form are worm-like, flat, lanceolate (meaning of a narrow oval shape that tapers to a point at each end), and pearly white. The rounded anterior end is wider than the posterior end. The body is encapsulated with a ringed cuticle. Two pairs of hooks are located medially and laterally (Lazo et al). Nymphs are often curved into a C-shape and less then one centimeter in diameter (John and Petri).
(Ravindram et al)
The life cycle of Linguatula serrata involves intermediate and definitive hosts. Above is a diagram of the L. serrata lifestyle from The Encyclopedic Reference of Parasitology by H. Melhorn (2004), and below is a description of the lifecycle from the same source:
Life cycle of Linguatula serrata: (1) Adults live in the nose of dogs (and rarely of man). (2) Embryonated eggs are set free via nasal mucus and/or feces. The thin outer is left out in drawings, since it disappears soon. (3) If intermediate hosts swallow eggs, the four-legged primary larva hatches and migrates via blood vessels to the inner organs. Humans may also become accidental intermediate hosts. (4-11) Larval stages 2–11 are included in a capsule of host origin and grow after molts. When final hosts ingest raw (or uncooked) meat of intermediate hosts, the adult stages develop inside the nasal tract.
Linguatuliasis often goes undetected. The disease may be suspected from the presentation of clinical signs and symptoms and confirmed by identification of linguatulids or eggs by microscopic exam (Slavashi et al). Nymphs rarely produce clinical symptoms and are discovered during autopsy, radiological exams, or surgical intervention (Lazo et al). This is because nymphs become calcified after death and thus visible on radiographs of the abdomen or chest. Treatment of larval pentastomiasis is most often unnecessary. In rare instances, severe laryngeal edema may require protection of the airway (John and Petri). Sneezing may be provoked to expel the worms or the worms may be removed mechanically (Mehlhorn). Management of Linguatulosis relies mostly in preventative measures. Avoidance of contact with dogs in tropical reasons is one prevention tool (Mehlhorn). Control also involves awareness of the disease in the community and preventing contamination of food and water from eggs by changing habits in the preparation of food and providing clean water for drinking and food preparation. Neither formal prevention strategies nor research toward the development of a vaccine have been initiated for Linguatulosis since it is a rare disease of relatively little mortality and morbidity significance (Ravindram et al).
Listed below are useful web links for reference on Linguatula serrata, Pentastomes, and other parasites:
Cannon, D. A. (1942) "Linguatulid Infestation of Man." Annals of Tropical Medicine, 36(4):160-167.
GIDEONonline.com. “Pentastomiasis—Linguatula.” 22 Feb 2009 <http://web.gideononline.com/web/epidemiology/index.php?gdn_form=ZGlzZWFzZT0xMTMwMA>
Institute of Tropical Medicine Antwerp. 2007. ITG. 15 Feb 2009 <http://www.itg.be/itg/DistanceLearning/LectureNotesVandenEndenE/imagehtml/ppages/CD_1094_066c.htm>
John, D.T., W.A. Petri Jr. (2006) Medical Parasitology. 9th ed. Elsevier, Inc. pp. 14, 336-337.
Lazo, R.F., E. Hidalgo, J.E. Lazo, A. Bermeo, M. Llaguno, J. Murillo, V.P.A. Teixeira (1999) “Ocular Linguatuliasis in Ecuador: Case report and morphometric study of the larva of Linguatula serrata.” The American Society of Tropical Medicine and Hygiene. 60(3):405-409.
Mehlhorn, H. (2004) Encyclopedic Reference of Parasitology, 2nd ed. Springer-Verlag Heidelberg.
Ravindram, R., Lakshmanan B., Ravishankar C., Subramanian H. (2008) “Prevalence of Linguatula serrata in domestic ruminants in South India.” Southeast Asian J. Trop. Med. Public Health. 39(5): 808-12.
Siavashi, M.R., M. Assmar, A. Vatankhah (2002) “Nasopharyngeal pentastomiasis (Halzoun): report of 3 cases.” Iranian Journal of Medical Sciences. 27(4):191-192.
Tappe D, Winzer R, Büttner DW, Ströbel P, Stich A, Klinker H, et al. (2006) “Linguatuliasis in Germany.” Emerg Infect Dis. 15 Feb 2009 <http://www.cdc.gov/ncidod/EID/vol12no06/05-1413.html>