Far more than 100 and probably more than 200 species of eukaryotes infect humans. By far the most important are parasites with terrestrial or freshwater life cycles. Nevertheless there are many marine species found in man, although none needs humans as obligatory hosts. The various infections including symptoms are discussed in the standard work edited by Rohde (Rohde 2005 , see also ).
Helminths (parasitic worms)
The largest number of marine parasite species found in humans are helminths, i.e., parasitic worms, such as nematodes (roundworms), trematodes (flukes) and cestodes (tapeworms). Characteristics of the groups, important for understanding the discussion below are as follows.
Most nematodes have separate sexes and pass through four larval stages (L1-L4), until sexual maturity is reached in the fifth stage. These stages are transformed into each other by four moults, i.e. the loss of the old cuticle and formation of a new one. In some cases the cuticle of the preceding stage remains as a sheath of the new stage.
Adult trematodes are usually hermaphroditic (i.e., the same individual has both male and female reproductive organs, which however may mature at different times), and they produce eggs in which the first larval stage, the ciliated miracidium, develops. This larva must get into the first intermediate host, almost always a mollusc, for further development to the sporocyst. Sporocysts produce daughter sporocysts or rediae, in which tailed cercariae are formed, which leave the host and either encapsulate outside the host or infect a second intermediate host, becoming metacercariae. Development of the sexually mature worm occurs after a final (definitive) vertebrate host has become infected. Species of the family Schistosomatidae have separate sexes and their cercariae penetrate actively through the skin of a vertebrate host.
All marine cestodes (tapeworm) infecting man belong with one exception to the Pseudophyllidea (family Diphyllobothriidae) which normally mature in marine mammals. Eggs are shed in the faeces. The first larval stage, the ciliated coracidium, develops in them. The coracidium hatches and penetrates into a copepod for further development, where it is transformed to the procercoid. In the muscles of fish which become infected by eating infected copepods, the next larva, the plerocercoid, develops. Mammals become infected by eating infected fish. Not rarely there are additional transport (paratenic) hosts, where larvae survive but do not grow and develop further.
Figure 1. Anisakidae larvae. (Aus der Wikipedia http://en.wikipedia.org/wiki/File:Anisakids.jpg).
Species of the genus Anisakis do not use seals but whales and dolphins as final hosts (“whale worms”) (e.g. ).
The symptoms of anisakiasis vary considerably, depending on which organs or tissues are infected (“stomach, intestinal and extraintestinal anisakiasis”). An acute and chronic form an also be distinguished. The former is mainly characterised by fast developing (two to seven hours after infection) abdominal pains, often accompanied by nausea and vomiting. In the mild chronic stomach anisakiasis pains are often weaker and can last for more than two years (if parasites are not removed by surgery). Almost all cases of intestinal anisakiasis are acute, usually with strong abdominal pains, nausea, congestion and diarrhea. In most extra-intestinal cases symptoms are localized and mild (Nagasawa 2005 ).
Infections are easily preventable by cooking of hosts, or by freezing at -20o C for one to several days (Nagasawa 2005 ). The probability of acquiring an infection can be reduced by removal of viscera of fish a short time after capture, which prevents migration of larvae from the intestine into the tissues, although some larvae are already in the tissues (Williams und Jones 1976 ). The effectiveness of control measures has been demonstrated by the fact that no new cases of human infections occurred after the Netherlands government had introduced a law that made it compulsory to freeze fish before sale as “green herring” (raw herring) (Rae 1972 ). However, in many countries fresh fish are preferred over frozen ones.
Trichinosis is caused by infections with species of the nematode Trichinella. Heavy infections can cause death and were, for example, quite common in Europe in the 19th century, until strict inspections radically reduced prevalence of infection. The most widespread infection mechanism is eating of insufficiently cooked pork. Mature worms live only for a short time in the duodenum, where they copulate and produce live larvae, which migrate into the blood system. Larvae of the first stage (i.e., before moulting) encapsulate in the striated muscles. Some genotypes live freely in the muscles without forming capsules. Marine mammals are exclusively infected with the species Trichinella nativa. The species is tolerant to freezing, whereas the forms transmitted in pork are not.
Cases of Trichinella in marine mammals are restricted to the circumpolar arctic, where 60% of polar bears are infected in some regions. Walrus (also up to 60%) and more rarely whales and seals also serve as hosts. Trichinella acquired from marine mammals is an important source of human infection. Walrus and polar bears are the most important sources. Symptoms depend on infection intensity. Importantly, even freezing at –20o C for four years did not kill all larvae (Forbes 2005 ).
Normal final hosts of the rat-lungworm Angiostrongylus cantonensis are various rodents, among others rats. The parasite is no genuine marine parasite, but uses terrestrial and freshwater animals in its life cycle. However, some marine invertebrates are transport (paratenic) hosts which can transmit the infection to other hosts. Humans are abnormal hosts who contain the third larval stage. The worms do not mature in humans. Originally the species was restricted to the Indo-Pacific region, but has been introduced into other tropical and subtropical regions. – Mature worms live in the lung arteries of rodents (at high infection intensities also in the right ventricle). They produce eggs, from which larvae hatch in the lung arteries and capillaries. They migrate up the trachea, are swallowed and shed in the faeces. Terrestrial and freshwater molluscs eat the larvae or are infected by external penetration of the larvae. The larvae develop within a few weeks to the third stage, which is infective to rodents. In the rodents, the larvae reach the surface of the brain via the blood or nervous system. After a few weeks they migrate into the lung arteries (Overstreet 2005 ).
Various brackish water and marine fish as well as invertebrates (e.g., Cheng, cit. in ) could be experimentally infected. Shrimps of the families Palaemonidae and Penaeidae in aquaculture are probably the most important transport hosts in the sea, and oysters and marine mussels (Mercenaria) are suitable intermediate hosts (Overstreet 2005 ).
The syndrome caused by the worms is eosinophilic meningoencephalitis (or eosinophilic meningitis), an inflammation of the cerebral membranes with an accumulation of eosinophilic white blood cells. In extreme cases there may even be mental disturbances and death. Very strong headaches, paralysis, vomiting and fever are only some of the other possible symptoms. Freezing and heating kills the larvae (Overstreet 2005 ).
Schistosome dermatitis (cercarial dermatitis)
Larvae of several species of the trematode family Schistosomatidae, which normally infect birds and (non-human) mammals, attempt penetration through the skin of humans in certain waters. Since man is an abnormal host, they die without obtaining sexual maturity, but can cause often severe inflammatory reactions of the skin. In the sea, species of Austrobilharzia (Figure 2), Ornithobilharzia and Gigantobilharzia as well as probably other genera are responsible. They all use birds as “normal” final hosts. Of special interest is Austrobilharzia (A. terrigalensis, A.variglandis) which use many species of molluscs as intermediate hosts.
Figure 2. Austrobilharzia terrigalensis (Trematoda, Schistosomatidae) from the blood vessels of the gull Larus novaehollandiae at Heron Island, Great Barrier Reef. The thin male (arrow) lies in a fold of the much broader female. Cercariae of this species cause a cercarial dermatitis. Original Klaus Rohde. © Klaus Rohde
Infections occur especially in calm coastal waters like lagoons or estuaries, which can be explained by the behaviour of the schistosome larvae. They swim to the surface of the water and wait there until a suitable host appears. They then penetrate into the skin, where they cause prickling irritations, lasting for about one hour. Urticaria and other skin reactions which can develop to liquid filled bladders, are characteristic. Secondary infections may occur, and lesions are often pigmented and can last for 10 days or even weeks or months. A first infection generally leads to only weak reactions, repeated infections lead to much stronger reactions including general symptoms such as fever and oedemas (Walker 2005  also Rohde 1993 ). Contact with larvae of species known to cause a dermatitis sometimes cause no symptoms, shown by experiments with cercariae of Austrobilharzia terrigalensis (Rohde 1993 ).
Humans may be infected with a large number of helminth species by ingesting larvae (plerocercoids of tapeworms, metacercariae of flukes) in insufficiently cooked marine animals. Raw, salted, marinated or only weakly cooked fish and invertebrates, such as molluscs, are traditionally liked delicacies in many countries (among others Korea, Japan, Hawaii and other Pacific islands). Widespread are sushi and sashimi (raw fish), originally Japanese delicacies, but now popular world-wide. In Polynesia freshly caught fish, such as tunas or bonitos, are cut into small pieces, washed in seawater and eaten with freshly pessed lemon juice. Laird (1961 ), for example, has shown that human infections with numerous trematodes are frequent in Japan, the Philippines and Polynesia.
Trematodes transmitted by marine or brackish water animals use without exception snails as first, and molluscs and fish containing the metacercariae as second intermediate hosts. Infections are restricted to estuaries and coastal regions, and all species are small. With few exceptions species belong to the family Heterophyidae (Figure 3) (more rarely to the Echinostomatidae and Gymnophallidae). Prevalence of infection can be very high. For example, in a Korean village 75% of the population was infected (references in Blair 2005 ). Infections with such flukes are probably much more common than usually assumed, because symptoms, if they are present at all, are often weak with little specificity, in spite of the often enormous infection intensities. Thus, almost 70,000 worms of three species were demonstrated in a Korean patient who had relatively minor symptoms: occasionally light pains in the stomach region, diarrhea and bad digestion. On the other hand, worms were also found in patients with serious symptoms like pancreatitis (inflammation of the pancreas), although it is not clear whether the parasites were the causes of the symptoms. In rare cases the small worms may leave the intestinal canal and they, or more frequently their eggs, may cause embolisms in the brain, spinal cord and heart, sometimes with fatal consequences (Blair 2005 ). Of special interest is that the fluke Nanophyetus salmincola contains a hyperparasitic microorganism, Neorickettsia helminthoeca, which causes a lethal infection in canids (dogs and related species) (“salmon poisoning disease”). Although human infections with this trematode are not known, a related species in Siberia infects almost 100% of humans in some regions. Infection is acquired in freshwater, but metacercariae have been found in marine fish (salmonids), where they can survive for several years (references in ).
Figure 3. Heterophyid trematode. Original Klaus Rohde. © Klaus Rohde
Tapeworms, with one exception (a trypanorhynch) belong either to the genus Diphyllobothrium, or (some) to Diplogonoporus (Figure 4). Natural final hosts are whales and seals. Life cycles include copepods as first, and fish (containing the plerocercoid larva infective to man) as second intermediate hosts. Transport host may also be included. Most important for humans are Diphyllobothrium pacificum and Diplogonoporus spp. Symptoms are diarrhea, abdominal pains, anorexia and general weakness. Kikuchi et al. (cited in ) report an accidental infection with a larval trypanorhynch in Japan, apparently acquired by ingestion of a raw cephalopod (Figure 5).
Figure 4. Anterior end of a pseudophyllidean tapeworm. Note the simple scolex with a groove. Original Klaus Rohde. © Klaus Rohde
Figure 5. Trypanorhynch larva from marine teleost fish. Note the elaborate scolex with tentacles bearing hooks. (This is not the species that had infected a human!). Original Klaus Rohde. © Klaus Rohde
Furthermore, ingested Acanthocephala and Nematoda (in addition to those causing anisakiasis) may occasionally infect humans (for details and references see Rohde 1993 ). Deardorff et al. (1986 ) describe a case of human infection with a sexually mature female roundworm Philometra sp., which had penetrated through the wound of the hand of a fisherman.
Unicellular eukaryotes (Protista)
Marine species infecting man belong to the Microsporidia and Apicomplexa, and possibly to the flagellates. Microsporidia are found in almost all phyla of invertebrates and in five classes of vertebrates. To date more than 1300 species have been described, but this is only a small proportion of the extant species, since most potential hosts have never been examined. Microsporidia are intracellular parasites and form infective spores (Figure 6). At least 14 species in six genera (only some of them in the sea) infect humans, most however only immune-deficient such as AIDS patients. “Pleistophora”, for example, parasitises poikilothermic animals, especially marine and freshwater fish, but it was also found in a human with weakened immune reactions. An increasing number of species resembling species in fish are found in immune-incompetent humans. Fish, and also crustaceans, must be considered to be possible sources of infection (Freeman 2005 ).
Figure 6. Mature spore of Vairimorpha cheracis, a microsporidian parasite of the Australian yabby, Cherax destructor, transmission electron micrograph. Note the nucleus, posterior vacuole and sections through 11 coils of polar filament. A new host cell is infected by extrusion of the spore’s content into the cell through the everted filament. © Dr. Elizabeth Moodie.
Marine Apicomplexa belong exclusively to the Coccidia. Infection occurs by ingestion of oocysts. Again, mainly immune-defective persons become infected. The species Cryptosporidium parvum (and related species of the same genus) cause cryptosporidiosis in man. Oocysts are ingested in polluted water and cause serious diarrhea. Although the species are typical freshwater organisms, infective oocysts can be washed into coastal waters and survive there for up to a year. Marine mussels and oysters can accumulate oocysts and ingestion of such potential carriers should therefore be avoided by immune-defective persons (Freeman 2005 ). Gomez-Bautista et al. 2000 ), for example, have shown that mussels (Mytilus gallo-provincialis) and cockles (Cerastoderma edule) on the coast of northwestern Spain contained oocysts of this species which were infective to newly born mice.
The primitive protistan (“flagellate”) Giardia infects various vertebrates, among them man, usually in freshwater. However, resistant resting stages were isolated from marine mussels. The possibility can therefore not be excluded that man can become infected by eating infected marine molluscs (Freeman 2005 ). Symptoms include serious diarrhea.
Webb et al. (1985 ) described a case of human infection with the mite Orthohalarachne attenuata, which normally occurs in the nostrils of walrus. In man, the iris of the eye was infected, leading to damage to the cornea and eye irritation. Apparently, infection was acquired by close contact with walrus.
Among the fishes, eel-like Cyclostomata (lampreys) occasional attack humans as temporary parasites, i.e., they attach themselves by means of their oral disk covered with many horny “teeth” (Fig.7) to the body and ingest blood and tissue.
Fig. 7. Oral disk of the sea lamprey, Petromyzon marinus. GNU free documentation license.
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Aspidogastrea I: http://knol.google.com/k/klaus-rohde/the-aspidogastrea-a-parasitological/xk923bc3gp4/13#
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Copyright note and Acknowledgement
This article is based on, but strongly modified from my report originally published in the German Wikipedia (link here). It does not contain any changes by others. I wish to thank Dr. Elizabeth Moodie for the electron micrograph of the microsporidian (Figure 6).