I What is it?

Nanophyetiasis, caused by Nanophyetus salmincola, is a food-born intestinal trematode endemic to the Northwestern United States and certain areas in Siberia.  Commonly called “Salmon Poisoning”, and hence the name salmincola, Nanophyetiasis can be caused by ingesting raw, or undercooked salmonid fishes carrying the worm.  While the disease normally affects dogs and other fish eating birds and mammals, Nanophyetiasis has also been observed in humans.

 

II Agent of Transmission

The agent of transmission of Nanophyetiasis in North America is the Trematode Nanophyetus salmincola.  In Siberia the agent is Nanophyetus schikhobalowi. The full taxonomic classification for the North American species is Kingdom: Animalia Phylum: Platyhelminthes Class: Trematoda Order: Digenea Family: Troglotrematidae Genus: Nanophyetus Species: Salmincola.[i]


III Synonyms

Nanophyetiasis, the disease caused by Nanophyetus salmincola, has been called by different names over time.  Most commonly it is referred to as “Salmon Poisoning” or “Fish Flu” due to the fact that symptoms usually arise after the ingestion of fish, particularly salmonid species.

 

IV History of Discovery

The study of Nanophyetiasis was first undertaken mainly by those who were interested in sicknesses of canines.  It was observed that dogs who were fed uncooked fish, particularly Salmon, soon became sick and eventually died.  This sickness was noted as early as 1814 by an Astoria, Oregon newspaper[ii].  Throughout the history of the study of this trematode it was thought, by various researchers working as early as 1855, to be: a virus, a bacterium, an ameba, mechanical destruction and a rickettsia.[iii]  It was discovered to be a fluke in 1926 by E. A. Chaplin, who gave it the name Nanophyetus salmincola, which was later amended to its current form.  Two Russian scientists, Skrjabin and Podjapolskaja, made similar discoveries about the Siberian form, Nanophyetus schikhobalowi, in 1931.  While the ability for human infection by the trematode was demonstrated by the self-infection of researcher in 1956, the first reported human cases surfaced only in the late 1980’s.[iv]

 

V Clinical Presentation

Most often those infected with Nanophyetiasis are asymptomatic, presenting no abnormal symptoms that would cause one to seek medical treatment.  Of those who do seek medical treatment, the most common symptoms are increased bowl movements and eosinophila.  Other symptoms include nausea and vomiting, weight loss, fatigue and diminished appetite.[v]

 

 

 

 

VI Transmission

Nanophyetus salmincola is transmitted most commonly by the ingestion of  raw, undercooked, or smoked salmon or steelhead trout.  Usually this is meant to be ingestion of the muscle of the fish but there have been cases reported in which the suspected agent of transmission was steelhead roe.  Researchers hypothesize, in fish with especially high worm burdens, that the N. salmincola may migrate to many of the fishes tissues, not just the muscle tissue.  In a  case in 1990 Nanophyetiasis was diagnosed in an individual that is thought to have acquired the disease by simple handling of fresh-killed salmon.  The infected individual, ironically, was a researcher studying N.salmincola in juvenile Coho salmon, had inadvertently initiated the infection by hand-to-mouth contact during the 3 month long study. [vi]

 

VII Reservoirs

N. salmincola requires three hosts in order to complete it life cycle.  The first intermediate host is the small stream snail Oxytrema silicula.  This snail is found in the rivers and streams west of the Cascade Mountain chain from the Canadian border to northern California. Studies have shown that, depending on the time of year, as much as 52% of Oxytrema silicula harbor the N. salmincola.[vii] The second host for N. salmincola is one of a number of salmonid and some non-salmonid species of fish native to the Northwestern United States.  Also, the Pacific giant salamander also serves as a secondary host, albeit a rare one. Researchers have shown that the trematode does have an adverse affect on its fish host.  When the parasite is migrating through the tissues of the fish it greatly impairs the swimming ability of the fish, making it swim almost half as fast as normal.[viii]  After the parasite has encysted, however, the fish is little affected.

 
The definitive hosts are fish-eating birds and mammals. There are 32 known species of definitive hosts for N. salmincola
, including three bird species. The most common definitive hosts are raccoons, skunks and minks, but also such animals as rats, otters and weasels.[ix][x]

 

With regard to the Siberian variety of the disease, caused by Nanophyetus schikhobalowi, its reservoirs and hosts follow the same pattern, going from snail to fish to mammal or bird, as the North American variety, only differing in the actual species involved.

 

VIII Vector

The vector  of Nanophyetiasis to humans is one of any number of salmonid fishes, most commonly Salmon or Steelhead Trout.  Consuming of these fishes or hand-to-mouth exposure has been shown to transmit the disease.

 

IX Incubation Period

After initial exposure to N. salmincola it takes about one week for eggs to be detected in the stool.


X Morphology

The adult trematode worm is approximately 0.8 – 2.5 mm long by 0.3 – 0.5 mm wide.  They are hermaphroditic, having both male and female sex organs.  N. salmincola also posses a ventricle and oral sucker that it uses to move around the intestine of  a host.[xi]

 

XI Life Cycle

Moving clockwise from top: Lynx acquires N. salmincola then defecates near river or lake.  Eggs are deposited in the water where they hatch  and miracidia infect snail host. Miracidia develop into cercariae and leave the snail host to find the fish host. Once in the fish the cercariae transform into metacercariae.  The Lynx then eats the fish and the cycle begins again.

 

 

The life cycle of Nanophyetus salmincola is typical to the trematode family. Adult worms, found in vertebrate hosts such as raccoons, skunks, and humans,  produce eggs that are then shed in feces. Many of these definite hosts defecate near streams and rivers, which is important to the life cycle of N. salmincola because the eggs found in the feces are allowed to enter the aquatic environment where they find their next host, the snail Oxytrema silicula. Once the eggs enter the water it can take from 31-175 days to hatch when in ideal situations.  As river or lake temperatures warm, hatching rate decreases.[xii]

  The newly hatched miracidia locate the snails and take up residency in their new hosts. Miracidia measure 0.087-0.105 x 0.021-0.042 mm.[xiii] Snail infection has been shown to occur in both fresh water and brackish water (up to 20š salinity).  Usually only large snails, those bigger than 2 cm, are infected. Within the snail N. salmincola then develops into a rediae.  The rediae are found in all tissues of the snail, but primarily in the gonads and digestive glands, severely damaging the former.  The snail is forced to deal with parasitic wastes and N. salmincola  actively uptakes glycogen and lipids from the snail; the burden put on the snail by the trematode is substantial.[xiv]

Inside the Oxytrema silicula host the rediae then develop into cercariae in 7-15 days. Cercariae leave their snail host by passing out through the mantel cavity and being taken out by water current.  Numbers of cercariae leaving the snail increases as the temperature increase and about five times as many cercariae leave the snail during the day than do during the night.[xv] Once cercariae leave the snail they set out in search of their second intermediate host, the fish.  When coming into close contact with a fish, closer than 1mm, the N. salmincola cercariae become excited and will penetrate the skin of the fish.   By doing so they cercariae loose their tails and become metacercariae .This process will take between 30 seconds and 5 minutes, but the cercariae do not crawl upon the exterior of the fish.[xvi] It is possible, however, for the fish to become infected by eating free-floating cercariae or snails harboring the parasite.  Once inside the fish the metacercariae will migrate to the fin base where it can enter the circulatory system.  Its destination is the renal tissue, where it will encyst its self.  Cysts are found throughout all tissues, however.


The definite hosts in the life cycle of Nanophyetus salmincola’s
are the previously mentioned vertebrates, usually raccoons, dogs, and minks.  Humans also fall into this category.  After ingesting the uncooked fish, the trematodes excyst and attach themselves to the upper small intestine of their host.[xvii]  From the small intestine N. salmincola will produce eggs to be passed out in the feces of the animal.  If the feces happen to be near or in water then the life cycle is able to begin again.

 

XII Diagnosis

     - History of raw fish consumption.

     - High contact with salmonid fishes, especially involving dissection or slaughter.[xviii]

Since each worm contains few eggs, stool samples regularly come back negative for eggs.  It is necessary, therefore, to use trichrome stained preparations in order to diagnose Nanophyetiasis. Eggs can be detected in stool about a week after ingestion.[xix] Eggs are light brown and measure 64-97 μx 34-55 μ .  They first appear in feces about 5-8 days after infected fish has been consumed.[xx]

XIII Therapy

There are a few treatment options for Nanophyetiasis infections. Three 2g doses of niclosamide or two 50 mg/kg doses of bithionol have been proven to be effective in combating Nanophyetiasis as well as three 25 mg/kg doses of praziquantel.   Research has proven mebendazole to not be efficacious.[xxi][xxii]

 

XIV Epidemiology

Nanophyetus salmincola is found in the U.S. states of Washington, Oregon and California, all west of the Cascade Mountains.  The trematode is limited to the endemic areas of its snail host, Oxytrema silicula, since the parasite is host specific to this snail. Nanophyetus schikhobalowi, another of the Nanophyetus genus that can cause Nanophyetiasis, is found in certain parts of Siberia.  Infection rates are extraordinarily high, 95%-98% of the population, in some Siberian villages that are dependant on fish for sustenance.[xxiii]

XV  Public Health and Prevention

Incidents of Nanophyetiasis in the United States have risen in the past twenty years due in part to changing preferences in cooking style.  Many more people are eating raw or “pan seared” fish and, therefore, exposing themselves to Nanophyetus salmincola. Some simple ways to combat the spread of this parasite are:

-       cooking fish thoroughly.

-       Freezing fish for 24 hours before consuming.

-       Molluscicides can be practical if used in small, specific areas.

-       Check fish for signs of cysts or cercariae entry.

-       Fish away from heavy snail habitats.

XVI Effects on Dogs

            Nanophyetiasis in dogs is much more serious than in humans.  Scientists noticed almost 200 years ago that dogs that consumed raw fish sometimes died rather quickly.  This “salmon poisoning” while associated with the trematode Nanophyetus salmincola is not caused by the worm.  The sickness is caused by Neorickettsia helminthoeca, a rickettsial bacteria that uses the N. salmincola as a host.[xxiv]  Only canines are susceptible to the disease.  Raccoons show a raised temperature and infection after being infected by the rickettsia, but both soon subside.[xxv]  The incubation period in dogs is 5-7 days, although it may take as long as 33 days.  After onset, there is a sharp fever coupled with anorexia, vomiting and dysentery.  The rickettsia attacks the canine’s lymph system causing enlarging and eventually hemorrhaging many of the lymph nodes.  The disease can spread to other tissues such as leucocytes. Death occurs 10-14 days after signs first appear.

XVII Useful Web Links

http://en.wikipedia.org/wiki/Nanophyetus_salmincola

http://www.stanford.edu/class/humbio103/ParaSites2003/Nanophyetiasis/Nanophyetiasis%20Home%20Page.htm

 

 



[i] David T. John and William A. Petri, Jr., Markell and Vogue’s Medical Parasitology (St. Louis: Elsevier Press, 2006), 203

[ii] RE Milleman and SE Knapp, “Biology of Nanopheyus Salmincola and “Salmon Poisoning” Disease” Advanced Parasitology, 8 (1970): 1-31

[iii] Elwin Bennington and Ivan Pratt “ Life History of the Salmon-Poisoning Fluke Nanophyetus SalmincolaThe Journal of Parasitology, 46-1 (1960): 91

[iv] Richard Eastburn and Thomas R. Fritsche and Charles A. Terhune, Jr. “ Human Intestinal Infection with Nanophyetus Salmincola from Salmonid Fishes” The American Society of Tropical Medicine and Hygiene, 36-3 (1987): 586

[v] Richard Eastburn and Thomas R. Fritsche and Charles A. Terhune, Jr. “ Human Intestinal Infection with Nanophyetus Salmincola from Salmonid Fishes” The American Society of Tropical Medicine and Hygiene, 36-3 (1987): 586

[vi] Lee W. Harrell and Thomas Deardorff “ Human Nanophyetiasis: Transmission by Handling Naturally Infected Coho Salmon” The Journal of Infectious Diseases, 161-1 (1990): 146

[vii] Richard Eastburn and Thomas R. Fritsche and Charles A. Terhune, Jr. “ Human Intestinal Infection with Nanophyetus Salmincola from Salmonid Fishes” The American Society of Tropical Medicine and Hygiene, 36-3 (1987):

[viii] Jerry A. Butler and Raymond E. Millemann. “ Effect of the ‘Salmon Poisoning’ Trematode, Nanopheyus Salmincola, on the Swimming Ability of Juvenile Salmonid Fishes” The Journal of Parasitology, 57-4 (1971): 860

[ix] Gary A. Gebhardt et al. “ Salmon Poisoning Disease II. Second Intermediate Host Susceptibility Studies” The Journal of Parasitology, 52-1 (1966), 54

[x] Gary A. Gebhardt et al. “ Salmon Poisoning Disease V. Definitive Hosts of the Trematode Vector, Nanophyetus Salmincola” The Journal of Parasitology, 52-1 (1966): 770

[xi] David T. John and William A. Petri, Jr., Markell and Vogue’s Medical Parasitology (St. Louis: Elsevier Press, 2006), 203

[xii] RE Milleman and SE Knapp, “Biology of Nanopheyus Salmincola and “Salmon Poisoning” Disease” Advanced Parasitology, 8 (1970): 11

[xiii] Ibid, 11

[xiv] Ibid,  16

[xv] Ibid, 16

[xvi] Ibid, 21

[xvii] Richard Eastburn and Thomas R. Fritsche and Charles A. Terhune, Jr. “ Human Intestinal Infection with Nanophyetus Salmincola from Salmonid Fishes” The American Society of Tropical Medicine and Hygiene, 36-3 (1987): 589

[xviii] Lee W. Harrell and Thomas Deardorff “ Human Nanophyetiasis: Transmission by Handling Naturally Infected Coho Salmon” The Journal of Infectious Diseases, 161-1 (1990): 146

[xix] Richard Eastburn and Thomas R. Fritsche and Charles A. Terhune, Jr. “ Human Intestinal Infection with Nanophyetus Salmincola from Salmonid Fishes” The American Society of Tropical Medicine and Hygiene, 36-3 (1987): 586

[xx] RE Milleman and SE Knapp, “Biology of Nanopheyus Salmincola and “Salmon Poisoning” Disease” Advanced Parasitology, 8 (1970): 1-31

[xxi] Richard Eastburn and Thomas R. Fritsche and Charles A. Terhune, Jr. “ Human Intestinal Infection with Nanophyetus Salmincola from Salmonid Fishes” The American Society of Tropical Medicine and Hygiene, 36-3 (1987): 590

[xxii] Thomas R. Fritsche et al. “ Praziquantel for Treatment of Human Nanophyeus salmincola Infection” The Journal of Infectious Diseases. 160-5 (1989): 896

[xxiii] Richard Eastburn and Thomas R. Fritsche and Charles A. Terhune, Jr. “ Human Intestinal Infection with Nanophyetus Salmincola from Salmonid Fishes” The American Society of Tropical Medicine and Hygiene, 36-3 (1987): 586

[xxiv] Ibid, 586

[xxv][xxv] RE Milleman and SE Knapp, “Biology of Nanopheyus Salmincola and “Salmon Poisoning” Disease” Advanced Parasitology, 8 (1970): 33