Pentastomes are obligate parasites of the lower and (less often) upper respiratory tract of vertebrates (Paré 2008), a lifestyle requiring a number of special physiological adaptations (reviewed by Riley and Henderson 1999). Pentastomes are particularly prevalent in the tropics and subtropics. Around 70% of definitive hosts of pentastomes (i.e., hosts in which the parasite becomes sexually mature) are snakes; smaller numbers of species infect crocodiles and lizards and just a handful are known to use amphibians (specifically, frogs and toads), turtles, birds, and mammals as definitive hosts. Known intermediate hosts include fishes, amphibians, lizards, snakes, insects, and mammals; a few species apparently have a direct life cycle. (Abele et al. 1989 and references therein; Riley and Henderson 1999 and references therein; Paré 2008 and references therein)
Pentastomes have flat, soft bodies and range in size from less than 2 to 15 cm in length, with females much larger than males. Adults of all pentastome species are easily distinguished from other parasites based on the two pairs of retractile hooks on either side of the mouth (Paré 2008). The cuticle covering the body is non-chitinous and is highly porous. The mouth, which lacks jaws, is often positioned at the end of a snoutlike projection and is typically connected to a muscular pumping pharynx used to suck blood from the host. Around 110 to 130 pentastome species have been described, including several that infest humans. (Riley 1986; Brusca and Brusca 2003; Margulis and Chapman 2010)
Both adult and larval pentastomes feed on blood from capillary beds (with the known exception of Linguatula species, which feed on cells and nasal secretions). The parasites attach to the host's mucosa with their hooks and in some genera the cephalothorax becomes embedded in the mucosa. As noted above, the life cycle of most pentastome species is indirect, involving multiple hosts. Females produce ova (eggs) that are coughed up, sneezed, or ingested and passed with feces. Once ingested by the intermediate host, the primary larva hatches and penetrates the gut wall. The larva then migrates, sometimes extensively, across the abdomen/coelom to finally encyst, often in visceral tissue, where it undergoes several moults to become an infective nymph. The cycle is completed when the intermediate host is consumed by the definitive host. Nymphs then excyst in the digestive tract (or, conceivably, in the mouth of the definitive host, Margulis and Chapman 2010) and migrate to the lungs, where they mature into young adults. Males traverse throughout the lung tissue and fertilize females early during the infection. Males usually do not live long, so mature pentastome infections in definitive hosts may well be all female. (Paré 2008 and references therein) Fertilization is internal. Pentastome eggs are tiny and lack yolks. The female's vagina is able to hold around half a million fertilized eggs; when full of eggs it can stretch to as much as a hundred times its usual volume. (Margulis and Chapman 2010)
Riley (1986) and Paré et al. (2008) thoroughly reviewed pentastomiasis in various vertebrate groups and should be referred to for detailed information on known definitive and intermediate host associations. Mammals are common intermediate hosts for many snake pentastomes. Mammals are definitive hosts for six species in the genus Linguatula (five of them parasites of carnivores) and for the recently described Rileyella petauri in sugar gliders (Petaurus breviceps). Among the Linguatula species is L. nuttali, found in the nasal passages of African lions (Panthera leo) and leopards (P. pardus), which cycles through the wild artiodactyl ungulates (hoofed mammals) on which the cats prey. Linguatula arctica is a parasite of semi-domesticated reindeer (Rangifer tarandus) in Scandinavia, and possibly of caribou, and is the only pentastome known to use an herbivore as a definitive host. (Paré et al. 2008 and references therein)
Pentastomes can infect humans, causing a disease known as visceral pentastomiasis. The parasites responsible can include the larval stages (nymphs) of Linguatula serrata, Armillifer species, or Porocephalus crotali. The majority of such infections involve species of Linguatula or Armillifer, with L. serrata and A. armillatus accounting for more than 90% of all reported pentastomiasis cases. The four species of Armillifer species causing pentastomiasis in humans are A. armillatus in Africa and the Arabian Peninsula, A. agkistrodontis in China, A. grandis in Africa, and A. moniliformis in Southeast Asia. Most cases of pentastomiasis have been reported from Africa, Malaysia, and the Middle East and less often from China and Latin America. In Europe and North America, the disease is only rarely encountered in immigrants and long-term travelers and the parasitic lesions may be confused with malignancies, leading to a delay in the correct diagnosis. The lifecycle of Armillifer species is believed to alternate between a snake - mouse cycle and one involving snakes and other mammals. Chen et al. (2010) investigated the lifecycle of Armillifer agkistrodontis in the lab. The time required for the completion of an entire lifecycle was about 14 months. Linguatula serrata, the most common pentastome reported from humans, parasitizes mammals and is not associated with reptiles; Armillifer and Porocephalus are the only reptile pentastomes that have been shown to infect humans (Paré 2008). Buckle et al. (1997) reported on a detailed lab study of the in vitro development of Porocephalus crotali, a pentastome infecting the Western Diamondback Rattlesnake (Crotalus atrox). (Paré 2008; Tappe and Büttner 2009; Chen et al. 2010).
In humans who accidentally serve as intermediate pentastome hosts, the infection develops when parasite ova are ingested from respiratory secretions or feces from the final hosts (dogs and other carnivores for Linguatula, several species of large snakes for Armillifer and Porocephalus). In the digestive tract of the human host, the tiny four-legged primary larva hatches and invades the viscera. After encapsulation by host tissue and several molts, the infective larval stage develops. In species infecting humans, the morphological appearance thereby changes and the nymphs finally resemble the adult legless vermiform pentastomes in shape. According to Tappe and Büttner (2009), in asymptomatic patients no treatment is necessary, since the parasites degenerate after approximately two years. Only in symptomatic infections with numerous parasites may a surgical approach have to be considered. There is no antiparasitic chemotherapy available for pentastomiasis. (Tappe and Büttner 2009)
A number of animal species can act as reservoirs for L. serrata. Adult worms are found in the nasal cavities of dogs, wolves, foxes, jackals, and other canids. Felids are not competent definitive hosts. A variety of prey mammals serve as intermediate hosts (e.g., cattle, goats, sheep). In endemic areas, humans become infected by domestic dogs. Ova expelled by sneezing, in nasal discharge, or possibly in the feces may contaminate food, fingers, and water sources. Infection may also occur when when humans ingest raw or undercooked viscera (e.g., sheep, goat, or even camel liver) containing encapsulated infective nymphs. Most Armillifer infections are acquired when undercooked snake meat is consumed, but may also involve ingestion of water contaminated with snake feces. Humans become accidental intermediate hosts. Infective nymphs exit the digestive tract and develop in the liver, mesentery, and intestinal wall. Humans are dead-end hosts and nymphs, even if long-lived, eventually die and calcify so that infection is often identified serendipitously through examination of abdominal radiographs or during a postmortem examination. Ingestion of live lizards for therapeutic reasons by humans in Southeast Asia was linked to subsequent subcutaneous pentastomid infection called “creeping disease” and was tentatively attributed to Raillietiella hemidactyli. (Paré 2008 and references therein)
The phylogenetic position of the Pentastomida has long been a matter of contention. Over the years, close relationships have been suggested with platyhelminths (both cestodes and trematodes), crustaceans, nematodes, chelicerate arthropods, annelids, tardigrades, and myriapods (see historical overview in Almeida and Christoffersen 1999). Although the position of this group in the animal tree remains somewhat controversial, a range of ultrastructural and molecular genetic data now indicate that this group falls within the arthropods, probably the crustacean arthropods and possibly within an early-branching crustacean lineage associated with the branchiurans (Abele et al. 1989 and references therein; Lavrov et al. 2004; Chen et al. 2010; but see Almeida et al. 2008). Cambrian pentastome fossils have been collected, consistent with molecular estimates that the pentastome lineage extends back around half a billion years (Sanders and Lee 2010).