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Pentastomiasis (porocephalosis, linguatulosis/linguatuliasis) 

Pentastomiasis (porocephalosis, linguatulosis/linguatuliasis)

Chapter:
Pentastomiasis (porocephalosis, linguatulosis/linguatuliasis)
Author(s):

David A. Warrell

DOI:
10.1093/med/9780199204854.003.0713_update_001

Update:

Taxonomy—phylogenetic trees indicate coevolution of pentastomes and other maxillopodan/branchiuran parasites with their vertebrate hosts: birds, snakes, mammals, and fish

Updated on 31 May 2012. The previous version of this content can be found here.
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Essentials

Pentastomiases or porocephaloses are zoonotic infections caused by maxillopod crustacean parasites (subclass Pentastomida).

Linguatula serrata (‘tongueworm’)—this is cosmopolitan, infecting upper respiratory tracts of the definitive hosts, canids. Nymphs discharged in nasal secretions are taken up by herbivorous animals, the intermediate hosts, which pass on the infection when they are eaten. Humans may be infected by eating raw liver and other offal of sheep, goats, and other animals, soon after which acute allergic obstructive nasolaryngopharyngitis (halzoun or marrara syndrome) may develop. Larvae can be found in sputum and vomitus.

Armillifer spp.—these are confined to Africa and South-East Asia, where they infect the respiratory tracts of snakes. Humans are infected by drinking snake-polluted water or by eating raw snake, a common practice in some communities. Most infections are asymptomatic, but massive infections may produce symptoms of an acute abdomen and are rarely fatal by causing intestinal obstruction or enterocolitis. Nymphs are detected at laparotomy or autopsy and (calcified) on abdominal radiographs.

Treatment and prevention—aside from standard measures for hypersensitivity phenomena, there is no specific treatment, although mebendazole has been suggested. Prevention is by thoroughly cooking all meat of whatever origin.

Introduction

The Pentastomida are currently regarded as a subclass of maxillopod crustaceans. Common names are ‘pentastomes’—because two pairs of hooks above the mouth give the impression of five stomata (Fig. 7.13.1) and ‘tongueworms’—because some resemble an animal’s tongue. They inhabit the respiratory tracts of vertebrates, feeding on blood and other tissues. There are about 100 living species in the orders Cephalobaenida (e.g. genus Raillietiella) and Porocephalida (e.g. genera Linguatula, Armillifer, Porocephalus, Leiperia, and Sebekia). About 10 species are recognized zoonotic parasites of humans, causing infections termed pentastomiasis, porocephalosis, linguatulosis, or linguatuliasis. In humans, visceral pentastomiasis is most often caused by Linguatula serrata or Armillifer armillatus. Nasopharyngeal pentastomiasis (‘Halzoun’ or ‘Marrara syndrome’) is caused by L. serrata. Phylogenetic trees have been constructed for all pentastome species infecting humans and animals from which sequence data were available. Pentastomes form their own branch close to the Branchiura (fish lice) and Remipedia (blind Crustacea). Armillifer armillatus is closest to A. agkistrodontis and P. crotali (Porocephalida), followed by L. serrata and Cephalobaenida (bird pentastomes). Pentastomes appear to have coevolved with other maxillopodan/branchiuran parasites and their vertebrate hosts: birds, snakes, mammals, and fish.

Fig. 7.13.1 Adult pentastomid showing mouth (arrowed) and lateral hooks giving the appearance of five stomata. Scanning electron micrograph, ×400.

Fig. 7.13.1
Adult pentastomid showing mouth (arrowed) and lateral hooks giving the appearance of five stomata. Scanning electron micrograph, ×400.

(Courtesy of Professor Viqar Zaman.)

Aetiology

Linguatula species

Linguatula serrata occurs in Europe, the Middle East, Africa, and North, Central, and South America. The names ‘linguatula’ and ‘tongueworm’ describe the numerous annular grooves and flattened shape, particularly of the adult female. Dogs, foxes, and wolves, the definitive hosts, harbour adults and nymphs in their upper respiratory tract and shed them in their nasal secretions, saliva, and faeces. Herbivorous animals ingest the ova, which hatch in the lumen of the gut, releasing larvae that burrow into the tissues and encyst. When these intermediate hosts are eaten by the definitive host, nymphs hatch from the cysts and migrate to the lungs and nasopharynx where they mature.

Clinical features

When humans ingest ova of linguatula, larvae hatch in the gut, burrow through its wall, migrate through the tissues, and encyst especially in the liver. Second- or third-stage larvae cause symptoms only by obstruction or compression, e.g. in biliary, gastrointestinal or respiratory tracts, meninges, or brain. In the anterior chamber of the eye, larvae have caused iritis and secondary glaucoma in the United States of America and elsewhere.

Ingestion of cysts containing third-stage larvae in raw liver or lymph nodes from sheep, goats, cattle, camels, and lagomorphs can cause nasopharyngeal pentostomiasis, known as ‘halzoun’ in Lebanon and ‘marrara syndrome’ in the Sudan. This has also been reported from other countries, including Greece, Turkey, North Africa, Egypt, and Jordan. In the human stomach, larvae escape from the cysts and migrate up the oesophagus to the nasopharynx mucosa. Within minutes to a few hours of eating the infected viscera, there is intense irritation of the upper respiratory and gastrointestinal tracts causing coughing, sneezing, rhinorrhoea, retching, vomiting, lacrimation, haemoptysis, epistaxis, cervical lymphadenopathy, transient deafness, difficulty in speaking, dysphagia, wheezing, dyspnoea, and oedema of the face and oropharynx. The larvae, which are 5 to 10 mm long, can be found in sputum and vomitus. Patients usually recover in 1 or 2 weeks, but fatal acute upper airway obstruction is reported. Clinical features suggest a hypersensitivity reaction. Flukes (Fasciola hepatica and Dicrocoelium dendriticum) and nematodes (Mammomonogamus laryngeus) ingested in raw sheep and goat liver, and aquatic leeches (Limnatis nilotica and Dinobdella ferox) (see Chapter 9.2) have been implicated in halzoun but cannot explain the classic syndrome. Very rarely, larvae may mature to adulthood in the human nasal cavity, causing bleeding and obstruction.

Armillifer (Porocephalus) species

These are also annulated, nonsegmented parasites (Fig. 7.13.2a). Adult males and the much larger females (up to 20 cm long) inhabit the respiratory and digestive tracts of snakes (Fig. 7.13.3), especially those of the genera Python, Lamprophis/Boaedon (African house snakes), Naja (cobras) (Fig. 7.13.4), Bitis (African vipers) (Fig. 7.13.2b), Bothrops (Latin American lanceheads) (Fig. 7.13.5), and other vertebrates. Ova are shed in the snake’s nasal secretions and are picked up by herbivorous mammals. Larvae encyst in the tissues of these intermediate hosts and will develop to the nymph stage if ingested by another animal, but develop to adults only in snakes. Humans may ingest ova by drinking water contaminated by snakes, or they may ingest living encysted larvae in raw or undercooked snake meat. This is eaten habitually or as part of ju ju rituals in Africa (Nigeria, Côte d’Ivoire, Benin, Cameroon, and the Democratic Republic of Congo(DRC)) and in South-East Asia, especially by the Temuan tribe of Malaysian aborigines. Ingested eggs hatch in the gut, releasing larvae which burrow into the tissues where they encyst as nymphs. The parasite species are A. armillatus and A. grandis in Africa and A. moniliformis in South-East Asia.

Fig. 7.13.2 Armillifer armillatus. (a) Left: two adults found in the lungs of (b) rhinoceros viper Bitis rhinoceros. Right: calcified nymph from the mesentery of a Ghanaian patient.

Fig. 7.13.2
Armillifer armillatus. (a) Left: two adults found in the lungs of (b) rhinoceros viper Bitis rhinoceros. Right: calcified nymph from the mesentery of a Ghanaian patient.

(Copyright D A Warrell.)

Fig. 7.13.3 Whip snake Demansia atra (Papua New Guinea) bringing up a pentastome.

Fig. 7.13.3
Whip snake Demansia atra (Papua New Guinea) bringing up a pentastome.

(Copyright Mark O’Shea.)

Fig. 7.13.4 (a) Pentastomes from the lungs of (b) an Egyptian cobra Naja haje.

Fig. 7.13.4
(a) Pentastomes from the lungs of (b) an Egyptian cobra Naja haje.

Fig. 7.13.5 Pentastomes found in the respiratory tract of lancehead vipers Bothrops spp., Manaus, Brazil.

Fig. 7.13.5
Pentastomes found in the respiratory tract of lancehead vipers Bothrops spp., Manaus, Brazil.

(Copyright D A Warrell.)

Epidemiology

The prevalence of infection can be judged by discovering calcified nymphs (Fig. 7.13.2) on radiographs of the abdomen and chest (Fig. 7.13.6). These appear as discrete, crescent-shaped, soft tissue calcifications, 4 to 8 mm in size. In West Africa they are seen particularly in the right upper quadrant and are situated beneath the peritoneum covering the liver. In Ibadan, Nigeria, they were seen in 1.4% of randomly selected straight abdominal films (7% in men aged 50–59 years). However, the prevalence of encysted nymphs or larvae at autopsy was 22.5% in DRC, 8% in Cameroon, 5% in West Africa and 45% in Malaysian Orang Asli. Cysts are found most commonly in liver (Fig. 7.13.7), mesentery, gut wall, peritoneum, spleen, kidneys, omentum and lungs. In Ibadan, pentastomiasis was the third most common cause of hepatic cirrhosis.

Fig. 7.13.6 Typical radiographic appearance of calcified nymphs of Armillifer armillatus in the abdominal cavity of a Ghanaian patient.

Fig. 7.13.6
Typical radiographic appearance of calcified nymphs of Armillifer armillatus in the abdominal cavity of a Ghanaian patient.

(Courtesy of Dr G M Ardran.)

Fig. 7.13.7 Encysted nymph/larva of Armillifer armillatus in human liver. The outer layer of the parasite (arrowed) lines the cyst wall. Acidophilic glands (ag), intestine (in), ×21.

Fig. 7.13.7
Encysted nymph/larva of Armillifer armillatus in human liver. The outer layer of the parasite (arrowed) lines the cyst wall. Acidophilic glands (ag), intestine (in), ×21.

(Armed Forces Institute of Pathology photograph, negative number 75–2703.)

Human infections with the larvae or nymphs of the following species of A. Armillifer have been reported:

  • A. agkistrodontis—China (in the snake Deinagkistrodon acutus)

  • A. armillatus (18–22 annular rings)—Africa: Egypt, Senegal, the Gambia, Ghana, Benin, Nigeria, Cameroon, DRC, and Zimbabwe

  • A. grandis—DRC, Côte d’Ivoire

  • A. moniliformis (30 annular rings)—Malaysia, Philippines, Indonesia, Tibet, and Australia

  • A. najae—India

Clinical features

Most infections are entirely asymptomatic. Migration of large numbers of larvae from the gut into the tissue may produce abdominal pain and obstructive jaundice. Massive infection, perhaps following ingestion of a gravid female, can cause acute abdominal symptoms prompting laparotomy at which hundreds of wriggling nymphs may be discovered beneath the visceral peritoneum. Serious inflammatory and obstructive effects have been described in the gut, peritoneum, liver and biliary tract, lungs, pleura, pericardium, central nervous system, and anterior chamber of the eye. These may be due partly to hypersensitivity. The few reported fatal cases had intestinal obstruction or haemorrhagic enterocolitis complicated perhaps by secondary Gram-negative septicaemia.

There is no convincing evidence of an association between Armillifer infection and colonic or other malignancies.

Other pentastomid infections

Human infections with Leiperia cincinnalis have been described in Africa and by Porocephalus crotali (from rattlesnakes) in North America. Subcutaneous infections by Railliettiella gehyrae and R. hemidactyli occur in Vietnam and by Sebekia species in Costa Rica. In Vietnam, infection with Railliettiella spp. results from swallowing small live lizards for medicinal purposes.

Diagnosis

The radiographical appearances of calcified pentastomid nymphs are distinctive (Fig. 7.13.6). They are not found in muscle, distinguishing pentastomiasis from cysticercosis. Pentastomes may be discovered at surgery or autopsy. In the liver (Fig. 7.13.7), intestinal wall, mesentery, mesenteric lymph nodes, peritoneum, or lung, viable encysted larvae or granulomas containing necrotic pentastomes or their moulted cuticles may be identified. Initially, encysted larvae excite little or no tissue reaction, but the granulomas are surrounded by hyalinized or calcified fibrous tissue. In tissue sections, pentastomes can be distinguished from helminths. Some patients have mild blood eosinophilia. Pentastomids have also been identified by consensus PCR and immunological tests are being developed.

Treatment

There is no specific treatment, although ivermectin, praziquantel, and mebendazole have been suggested. Obstruction and compression should be relieved surgically. Hypersensitivity phenomena should be treated with adrenaline (epinephrine), antihistamines, and corticosteroids.

Prevention

Pentostomiasis can be prevented by thoroughly cooking all meat of any origin and boiling or filtering drinking water. Eating sheep’s lymph nodes is proscribed by the Shi’ite Muslims of Lebanon.

Other zoonoses transmitted from reptiles to humans

The most important of these is salmonellosis transmitted to humans by the faecal–oral route or by scratches and bites, from chelonians (tortoises, turtles, terrapins) and from snakes and lizards, especially iguanas. In the United Kingdom, 38% of imported tortoises (Testudo spp.) contain salmonella. In the United States of America, where 8 million reptiles are kept as pets, contact with reptiles and amphibians accounts for an estimated 74 000 (6%) of the approximately 1.2 million sporadic human salmonella infections that occur there annually. The banning by the United States Food and Drug Administration of commercial distribution of small turtles has prevented an estimated 100 000 cases of salmonellosis among children each year. Although salmonellosis usually causes self-limiting gastroenteritis, septicaemia or meningitis may occur especially in infants and immunocompromised people. Species associated with reptile salmonellosis include S. enterica serotype Typhimurium, S. enterica serotype Pomona, and S. enterica subspecies diarizonae.

Other infections transmissible from reptiles to humans include Arizona hinshawii (in snake powder, Pulvo de Vibora, made from rattlesnakes), Plesiomonas shigelloides, Edwardsiella tarda, leptospirosis, Q fever, sparganosis, capillariasis, strongyloidiasis, mesocestoidiasis, and infestation with the mite Ophionyssus natricis. Potential zoonoses include mycobacteria, pseudomonas, other aeromonas species, proteus, and some togaviruses (such as western equine encephalitis in garter snakes in western North America) and herpesviruses.

Further reading

Brookins MD, et al. (2009). Massive visceral pentastomiasis caused by Porocephalus crotali in a dog. Vet Pathol, 46, 460–3.Find this resource:

Chen SH, et al. (2009). Multi-host model-based identification of Armillifer agkistrodontis (Pentastomida), a new zoonotic parasite from China. PLoS Negl Trop Dis, 4, e647.Find this resource:

Drabick JJ (1987). Pentastomiasis. Rev Infect Dis, 9, 1087–94.Find this resource:

Haugerud RE (1989). Evolution in the pentastomids. Parasitol Today, 5, 126–32.Find this resource:

Lai C, et al. (2010). Imaging features of pediatric pentastomiasis infection: a case report. Korean J Radiol, 11, 480–4.Find this resource:

Magnino S, Colin P, Dei-Cas E, et al. (2009). Biological risks associated with consumption of reptile products. Int J Food Microbiol, 134, 163–75.Find this resource:

Lavrov DV, et al. (2004). Phylogenetic position of the Pentastomida and (pan)crustacean relationships. Proc Biol Sci, 271, 537–44.Find this resource:

Palmer PES, Reeder MM (eds) (2001). Pentastomida. In: The imaging of tropical diseases with epidemiological, pathological and clinical correlation, Vol. 2, pp. 389–95. Springer, Berlin.Find this resource:

    Riley J (1986). The biology of pentastomids. Adv Parasitol, 25, 45–128.Find this resource:

    Schacher JF, Khalil GM, Salman S. (1965). A field study of Halzoun (parasitic pharyngitis) in Lebanon. J Trop Med Hyg, 68, 226–30.Find this resource:

    Tappe D, Büttner DW (2009). Diagnosis of human visceral pentastomiasis. PLoS Negl Trop Dis, 5, e320.Find this resource:

    Tappe D, et al. (2011). Diagnosis of human visceral pentastomiasis. Emerg Infect Dis, 17, 251–4.Find this resource:

    Warwick C, et al. (2001). Reptile-related salmonellosis. J Roy Soc Med, 94, 124–6.Find this resource:

    Yagi H, et al. (1996). The Marrara syndrome: a hypersensitivity reaction of the upper respiratory tract and buccopharyngeal mucosa to nymphs of Linguatula serrata. Acta Trop, 16, 127–34.Find this resource:

    Yao MH, Wu F, Tang LF (2008). Human pentastomiasis in China: case report and literature review. J Parasitol, 94, 1295–8.Find this resource:

    Yapo Ette H, et al. (2003). Human pentastomiasis discovered postmortem. Forensic Sci Int, 137, 52–4.Find this resource: