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The Superfamily Metastrongyloidea

The Metastrongyloidea is a moderately sized superfamily of bursate nematodes consisting of about 181 species classified into 46 genera and seven families (Anderson, 1978, 1982). The superfamily is confined to mammals and its species are most common in Artiodactyla (14 genera), Carnivora (14), Marsupialia (seven) and Cetacea (Odontoceti) (six). A number of genera occur in the Insectivora (five), Rodentia (three) and Primates (ten). Hares and rabbits (Lagomorpha) share Protostrongylus with the artiodactyls. Cattle and horses are devoid of metastrongyloids, their place being taken by Dictyocaulus spp. (Trichostrongyloidea) in these hosts.

Most metastrongyloids as adults occupy lungs of the host (e.g. Protostrongylus) but there are numerous important exceptions. Some members of the Protostrongylidae (Elaphostrongylus and Parelaphostrongylus) are associated with veins distant from the lungs and some members of the Angiostrongylidae occupy pulmonary and mesenteric arteries. Many members of the Pseudaliidae of Odontoceti, as well as all members of the Skrjabingylidae, occupy frontal sinuses.

Some species living in lungs deposit unembryonated eggs in the lung tissues or air spaces (e.g. Protostrongylidae, Aelurostrongylus abstrusus) whereas species living outside the lungs deposit unembryonated eggs that are carried to the lungs in blood (e.g. Angiostrongylus spp., Elaphostrongylus spp., Parelaphostrongylus spp.). Eggs develop in the lungs to first-stage larvae. Many metastrongyloids are ovoviviparous in that eggs develop into first-stage larvae in utero and female worms deposit these fully developed larvae into the lungs (e.g. Crenosomatidae, some Angiostrongylidae, many Filaroididae). Larvae of these species leave the lungs via the bronchial escalator and are swallowed and passed in the host's faeces.

In some metastrongyloids the lungs have been bypassed entirely. For example, in sinus worms (Skrjabingylidae, presumably some Pseudaliidae) larvae leave the sinuses, enter the throat and are swallowed. In addition, in certain Angiostrongylidae living in mesenteric arteries (Angiostrongylus costaricensis, A. siamensis) eggs embryonate in the intestinal wall and first-stage larvae apparently migrate into the lumen of the gut and are then passed in faeces of the host.

With the peculiar exception of the Metastrongylidae of Suidae which use earthworm intermediate hosts, a general feature of transmission in the Metastrongyloidea is the use of gastropods (usually terrestrial) in which development occurs to the third and infective stage; this was first discovered by Hobmaier and Hobmaier (1929c) in Muellerius capillaris. Many hosts (notably the artiodactyls) acquire their lungworm fauna from the accidental or deliberate ingestion of gastropods containing infective larvae. Species in Carnivora frequently utilize vertebrate paratenic hosts (e.g. amphibians, reptiles, rodents and shrews) to channel infective larvae to the definitive host. There are, however, some unusual exceptions to this general pattern of transmission in the Angiostrongylidae and the Filaroididae. In some species first-stage larvae are directly infective to the definitive host; these highly specialized species (Andersonstrongylus captivensis, Filaroides hirthi, Oslerus oslert) occur in skunks and canids. One species (Filaroides decorus) in sea-lions utilizes coprophagic fish as an intermediate hosts, and Otostrongylus circumlitus of seals uses American plaice, at least in Canadian waters.

Some recent observations seem to shed some light on these apparent anomalies in the transmission of the lungworms. It has been shown recently that first-stage larvae of Angiostrongylus cantonensis and A. vasorum can develop to the infective third stage in amphibians although the latter are not likely to be important in the transmission of these nematodes under natural conditions. This shows that some lungworms of carnivores have first-stage larvae with an innate ability to reach the infective stage in vertebrates. This may explain the fact that Andersonstrongylus captivensis (Angiostrongylidae), Filaroides hirthi and Oslerus osleri (Filaroididae) infect their hosts in the first stage, i.e. the mustelid or canid host serves as both intermediate and final hosts. The unusual ability of larvae to attain the infective third-stage in vertebrates explains how Filaroides decorus of sea-lions and Otostrongylus circumlitus (Crenosomatidae) of seals were able to stay with their hosts as the latter evolved from terrestrial into marine mammals. These highly adaptable parasites were able to replace the molluscan intermediate hosts with marine fish and thus ensure their survival in the new environment. Possibly lungworms of the Odontoceti survived the evolution of their terrestrial hosts into the marine environment by similar methods. Lungworms which failed to have an innate ability to reach the infective stage in vertebrates would presumably have been unable to survive in a marine host and would have become extinct.

There is considerable diversity in the migratory behaviour and development of metastrongyloids in the definitive host. Some infective larvae penetrate the gut and migrate in the lymph vessels and nodes to the heart, then pass to the lungs where they develop to adulthood (e.g. Cystocaulus ocreatus, Muellerius capillaris). Other species follow the hepatic portal system to the heart and lungs (e.g. Crenosoma spp.). Infective larvae of at least one species (e.g. Aelurostrongylus pridhami) penetrate the gut, enter the body cavity, cross the diaphragm and invade the lungs directly from the pleural cavity. Species like Parelaphostrongylus tenuis and Angiostrongylus cantonensis, living distant from the lungs, migrate as third-stage larvae to the central nervous system, where they develop to adulthood before moving to the definitive site in the host.

A number of lungworms undertake their migration to the definitive sites in the fifth or subadult stage. For example, species of Skrjabingylus as well as Filaroides martis reach the subadult stage in the gut wall and then undertake remarkably complex, highly directed migrations to the frontal sinuses and lungs, respectively. Subadult Angiostrongylus vasorum migrate from visceral lymph nodes to the hepatic portal system and then travel to the liver, heart and finally to the pulmonary arteries where they mature.