Nanophyetus salmincola is a food-borne intestinal trematode parasite prevalent on the Pacific Northwest coast. The species may be the most common trematode endemic to the United States.
The life cycle of the N. salmincola requires three hosts. The first intermediate host is an Juga plicifera stream snail. The second intermediate host is a salmonid fish, though some non-salmonid fishes also play a role. Lastly, the definitive host is most commonly a canid, though many other mammals are also definitive hosts, including humans. Transmission of N. salmincola to the definitive host occurs upon ingestion of parasite-infected fish.
The parasite is most known for its association with "salmon poisoning disease", which, left untreated, is fatal to dogs and other canids. However, canids are affected by the Neorickettsia helminthoeca bacteria, for which N. salmincola acts as a vector, and not by the parasite itself.
Very few known cases of naturally acquired human infection with N. salmincola are found in the literature, though it is likely that many cases are unreported, since most people are asymptomatic, or symptomatic with non-specific symptoms like gastrointestinal discomfort. Disease caused by N. salmincola, or nanophyetiasis, is easily preventable by thoroughly cooking fish before consumption. There are no known cases of human infection by the Rickettsia bacteria carried by N. salmincola.
A subspecific parasite, Nanophyetus schikhobalowi, is endemic to Siberia, where human cases of nanophyetiasis have been reported in scientific literature since 1931.Skrjabin, K. J., and Podjapolskaja, W. P., (1931).Nanophyetus schikhobalowi, n. sp., em neuer Trematode aus Darm des Menschen. Zlb. Ba/ct. I. Orig., 119: 294–297.
Discovery The first record of salmon poisoning disease (SPD) was reported in northwestern Oregon in 1814 when a writer for Henry's Astoria Journal noted the death of dogs after consumption of raw salmon.Min, Elijah. Nanophyetiasis. 2003. Stanford University. 12 February 2009. At first, investigators believed that SPD was caused by poisonous blood in the ingested fish.Thornton, J.Q. (1849). "Oregon and California in 1848". Vol.1, Harper & Bros. In 1911, small white cysts were observed in the kidneys of disease-causing salmon and trout, but the cysts were mistakenly identified as amebae. Small trematodes in the intestines of dogs that died after eating infected salmon were finally found in 1925 and the cysts present in the salmon were correctly identified as intermediate stages of the trematode.Donham, C.R. (1925a). Science 61:341. In an experimental follow-up study, researchers showed that the small intestinal parasite did in fact cause SPD in dogs, and that the cysts did develop into the adult worm found in the intestine.Donham, C.R., Simms, B.T. and Miller, F.W. (1926). J. Am. Vet. Med. Ass. 68:701–715
The trematode was first named by Chapin as Nanophyes salmincola in 1926, as a member of the family Heterophyidae.Chapin, E. A. (1926). N. Am. Vet. 7:36–37. Upon further examination of the morphology, Chapin reassigned the trematode to the family Troglotrematidae and renamed the parasite Nanophyetus salmincola, since Nanophyes was already taken.Chapin, E. A. (1928) J. Parasitol. 14: 60. Discussions regarding the correctness of classification of the parasite continued as the trematode received further scientific attention and its morphology and behavior was further scrutinized. Ultimately, Nanophyetus salmincola was agreed upon, though Troglotrema salmincola remains a synonym.
In 1931, Skrjabin and Podjapolskaja describe a similar parasite, Nanophyetus schikhobalowi, which was endemic to East Siberia. Argument regarding whether or not N. schikhobalowi and N. salmincola were the same or different species recurred until 1966 when the two were granted subspecific status in order to reflect their biological and geographic differences, but little significant morphological differences.Filimonova, L.V. (1966). Trans. Helminth. Lab. Acad. Sci. USSR 17, 240–244. Since its discovery, N. schikhobalowi has been known to naturally infect humans and research reveals surveys indicating rates of infection in endemic Siberian villages of up to 98%.
In contrast, N. salmincola was not recognized to be a source of an infection until a researcher purposefully infected himself in a scientific experiment in 1958.Philip, C. B. (1958). Proc. 10th Int. Congr. Ent., Montreal, 1956, 3:651–653. Besides Philip experimentally infecting himself with the North American N. salmincola, the first naturally acquired human intestinal infection cases were observed between September 1974 and October 1985. The study revealed 10 patients who presented with positive N. salmincola stool samples and either gastrointestinal complaints or otherwise unexplainable peripheral blood eosinophilia. 7 patients recalled ingestion of undercooked or raw fish. Of those who were not given effective treatment, symptoms and/or eggs in stools persisted for 2 or more months before spontaneously resolving. It was hypothesized that the movement, attachment, and irritation of the adult worms in the small intestine mucosa was the likely cause of gastrointestinal symptoms and peripheral eosinophilia.
Two years after the first 10 cases of human infection with N. salmincola were reported in 1987, Fritsche et al. reported ten additional cases of human nanophyetiasis.Fritsche TR, Eastburn RL, Wiggins LH, Terhune CA Jr. (1989) Praziquantel for treatment of human Nanophyetus salmincola (Troglotrema salmincola) infection. 160(5):896-9. Five presented with gastrointestinal complaints and the other five had unexplained peripheral eosinophilia. Nine out of ten recalled eating inadequately cooked fish. This time, praziquantel was the effective treatment of choice.
In 1990, the first case of human infection with N. salmincola without ingestion of raw or undercooked contaminated fish was reported. A man was infected through hand contamination while handling highly infected, fresh-killed, coho salmon. A diagnosis of nanophyetiasis was made based on gastrointestinal discomfort, peripheral blood eosinophilia and a positive stool sample. Treatment with praziquantel was effective.
None of the human cases of infection with either the North American or Siberian subspecies reveal infection by the Neorickettsia helminthoeca carried within the trematode, which was discovered in 1950. Infection by rickettsia helps to explain the more fatal outcome afflicting canids.
Clinical presentation in humans Upon infection with N. salmincola, humans are normally asymptomatic. If symptoms are present, they are usually non-specific and mistaken for indication of other gastrointestinal problems. Symptoms include "diarrhea, unexplained peripheral blood eosinophilia, abdominal discomfort, nausea and vomiting, weight loss, and fatigue". Eggs of N. salmincola appear in stools approximately one week after ingestion of infected fish.
Pathology in 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. Although only canines are susceptible to the disease raccoons show a raised temperature and lymphatic infection after being infected by the rickettsia, but both soon subside.RE Milleman and SE Knapp, "Biology of Nanopheyus Salmincola and "Salmon Poisoning" Disease" Advanced Parasitology, 8 (1970): 33 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 lymphnodes. The disease can spread to other tissues such as leukocytes. Death occurs 10–14 days after signs first appear.
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 who 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 who had inadvertently initiated the infection by hand-to-mouth contact during the 3-month-long study.Lee W. Harrell and Thomas Deardorff " Human Nanophyetiasis: Transmission by Handling Naturally Infected Coho Salmon" The Journal of Infectious Diseases, 161-1 (1990): 146
Reservoir The reservoirs for N. salmincola are raccoons, mink, and skunks. Reservoirs are organisms that harbor parasites within themselves without suffering any signs of pathology, and spreading the parasites through their natural behavior. For example, raccoons naturally spread N. salmincola because they frequently eat fish and defecate parasitic eggs in or near the water, where subsequent larval stages can continue their life cycle.
Vector Vectors are organisms that transmit parasites from one host to another. Juga plicifera stream snails are biological vectors for a larval stage of N. salmincola. Salmonid and some non-salmonid fish are vectors of the metacercariae of N. salmincola. Both fresh and ocean water fish can be parasitic vectors. Fish that act as second intermediate hosts are different species of the families Salmonidae, Cottidae, and Cyprinidae. Among the thirty-four natural and experimental secondary hosts found in scientific literature are the coastal cutthroat trout, rainbow trout, coho salmon, chum salmon, and kokanee salmon. More infection occurs in salmonid fish, rather than non-salmonid fish. In particular, salmonid fish of the genera Salmo, Oncorhynchus, and Salvelinus play a significant role in the N. salmincola life cycle.Witenburg, G. (1932) On the anatomy and systematic position of the causative agent of so-called salmon poisoning. J. Parasitol. 18:258–263. The parasite itself is also a vector for Neorickettsia helminthoeca.
Definitive hosts Definitive hosts include fish-eating birds and mammals. The most common definitive hosts are the domestic dog, cat, and red fox. Humans are also definitive hosts for N. salmincola. A long list of experimental definitive hosts include the hamster and wood rat. An experimental study failed to infect two white rats and two white mice. Trematodes exist along the whole length of the small intestine in smaller animals like hamsters, while they exist only in the upper end of the small intestine in larger animals like dogs.
Incubation period After ingestion of fish infected with N. salmincola, it takes about 1 week for symptoms to occur, namely for eggs to be detected in the stool.
Morphology Eggs of N. salmincola are light brown, ovoid, and operculate at one end, with a small blunt projection at the other end. They measure 0.087 mm to 0.097 mm by 0.038 mm to 0.055 mm. There are normally 5 to 16 eggs in the uterus, and their heaviness allows them to sink rapidly in water.