Worms and Other Stuff in the Mouth
special report
"In Mexico we have a word for sushi: Bait." —Jose Simon
Early on a recent saturday morning, a 49-year-old male called because, while sitting comfortably reading his morning newspaper, he found a live, wriggling worm in his mouth. He felt otherwise well, but did recall that two nights earlier, he had difficulty getting to sleep because of a sensation that something was caught in the back of his throat. He denied abdominal pain, vomiting, or diarrhea, but indicated he took lansoprazole to treat gastro-esophageal reflux disease.
He had no pets and had no relevant travel history. He had no unusual dietary habits, but did often eat sushi and, in addition, ate salmon at home several days prior to his phone call; he believed the salmon had been well cooked.
Upon examination, the worm was a third-stage larva of Anisakis simplex, a "sushi worm."
Comment by Stan Deresinski, md, facp
Although affected patients somehow miss the humor, nothing elicits attempts at jocularity by medical authors like the sushi worm, the cause of anisakiasis. (See Table 1.) Human anisakiasis (also called anisakidosis) is the result of the accidental ingestion of the larvae of one of several anisakid nematodes. (See Table 2.) A. simplex and, with lesser frequency, Pseudoterranova decipiens have been responsible for all reported North American cases.1-4 All the etiologic agents of anisakiasis belong to the family Anisakidae of the superfamily Ascaroidea.5
The infection may be invasive or noninvasive and symptomatic cases of anisakiasis may present in one of several ways. As the result of the occasional cephalad migration of the larval nematode from the stomach, it may be discovered as a consequence of its causing a tickling sensation in the oronasopharynx ("tingling throat syndrome"). The worm has also been discovered extruding from the nares of a child and it may also be expelled as the result of coughing or vomiting. Each of these presentations may occur from one day to two weeks after ingestion of the parasite. An anisakid worm has also been found in the resected tonsil of a child with chronic recurrent tonsillitis.6
Having found the stomach a salubrious environment, the parasite may attempt to burrow into the gastric mucosa, with resultant acute abdominal pain, vomiting, and hematemesis occurring within less than an hour of ingestion of the worm.7-9 Leukocytosis is common but significant eosinophilia is not. Patients may present with severe chest pain that must be distinguished from cardiac ischemia.10,11 Although chest pain is usually due to gastric involvement, the parasite may also burrow into the esophageal mucosa.12 Anisakiasis may also be associated with a "vanishing tumor" of the stomach or, less frequently, other sites in the gastrointestinal tract.5 Therapy of gastric (or esophageal) anisakiasis consists of endoscopic extraction of the parasite. Endoscopic examination of 87 patients with gastric anisakiasis found that 55% of the worms were found in the greater curvature.13
| Table 1-Some Notable Titles of Medical Articles About Sushi |
| "If you knew sushi like I know sushi"53 |
| "Sushi syncope schusser gets wedeler’s valve at Vail"54 |
| "Hot tubs, sex, sushi, and infectious diseases"55 |
| "Anisakiasis: Revenge of the sushi parasite"56 |
| "Hold the sushi"57 |
"Horseradish horrors: Sushi syncope"58
Organisms that make their way farther along the gastrointestinal tract may burrow into the intestinal wall to the level of the muscularis mucosae and, occasionally, may penetrate transmurally and find their way to the peritoneal cavity. Worms that have penetrated tissues elicit a granulomatous response and die, not necessarily in that order. This may result in intestinal obstruction, an omental mass lesion, fever, and pain.14-16 Intestinal symptoms usually begin within 48 hours of ingestion of the parasite and may last one to five days. Intestinal obstruction is associated with segmental involvement of the small bowel.17 Intestinal anisakiasis or involvement of mesenteric lymph nodes may each cause findings that can be confused with acute appendicitis.16,18 A. simplex has caused peritonitis in a patient undergoing continuous ambulatory peritoneal dialysis.19 Anisakids that are not ejected anally and do not penetrate tissue are eliminated spontaneously within three weeks of infection.
In addition to these direct effects of the parasite, reports from Spain strongly suggest that, despite the usual absence of significant eosinophilia, anasakid worms may be responsible for a variety of allergic manifestations, including urticaria and anaphylaxis.20 A study of 26 patients who had urticaria or angioedema 20 minutes to 23 hours after eating raw or undercooked fish, only one-half of whom had abdominal symptoms, found a high frequency of IgE antibody and positive skin prick tests to A. simplex antigens, relative to controls.21 Serologic studies have demonstrated an association between sensitization to A. simplex and some cases of eosinophilic gastroenteritis.22
Patients with allergic manifestations after eating infected fish may subsequently ingest the same species of fish without elicitation of symptoms, if the fish are not infected.23 On the other hand, allergic reactions may subsequently occur as the result of ingestion of fish containing nonviable A. simplex.
| Table 2-Anisakid Nematodes Implicated in Human Infections1 |
| Anisakis simplex (herring worm)* |
| Pseudoterranova (Phocanema, Terranova) decipiens (cod or seal worm)* |
| Contracaecum spp. |
| Hysterothylacium (Thynnascaris) spp. |
| *Reported from North American cases |
Epidemiology
Human infection by anisakid nematodes is the consequence of the ingestion of infested, raw, undercooked, or insufficiently cured fish and shellfish. The yearly number of identified and reported cases in the United States is fewer than 10, with Hawaii and California contributing the most cases. In contrast, more than 1000 cases are reported annually in Japan.1
Sea mammals become infected with third-stage larvae by ingesting fish or squid containing the parasite. A. simplex predominantly affects dolphins, porpoises, and whales, while P. decipiens affects seals, fur seals, walruses, and sea lions. The anisakid matures to the adult stage in the stomach of the sea mammal and eggs are subsequently excreted in the feces. These are eaten by small crustaceans, such as krill, and start their way up the food chain once again. Larvae of A. simplex are found predominantly in herring, salmon, cod, mackerel, and squid, while P. decipiens, in addition to infesting cod, are also found in halibut, flatfish, greenling, pike, bonito, Alaskan pollack, and red snapper (Pacific red snapper is actually a rockfish). Humans become infected by ingestion of fish containing viable larvae.
Diagnosis
The diagnosis of anisakiais may be made by examination of an expelled or extracted worm.24 The third-stage larvae of A. simplex are 19-36 mm in length and up to 0.1 cm in diameter. They are white or milky in color and have a long stomach and intestine with absent cecum, and a blunt tail. The anterior portion of the head contains three bilobed lips, and a small boring tooth just dorsal to an excretory pore; near the rectum are three anal glands. The third-stage larvae of P. decipiens, which are yellow or brownish as the result of hematophagy, are 25-50 mm by 0.3-1.2 mm. They have an anteriorly projected cecum.
The diagnosis of gastric anisakiasis is best made at endoscopy, a procedure that allows definitive therapy, i.e., extraction of the parasite. If radiographic examination is, however, performed, it may reveal mucosal edema, pseudotumor formation, and a threadlike filling defect approximately 30 mm in length representing the worm.25
Abdominal ultrasound examination of patients with small intestinal anisakiasis often reveals ascites, small bowel dilatation, and focal edema of Kerckring’s folds.26 Double-contrast radiographic examination of patients with colonic anisakiasis may reveal right-sided luminal narrowing and thumbprinting; due to mucosal edema the worm may also be visualized.27 Colonic anisakiasis may simulate carcinoma.28 The worm may be extracted during colonoscopy.29
Histologic examination of tissue removed at surgery reveals an eosinophilic granuloma with a larva with Y-shaped lateral chords without the lateral alae (seen in Ascaris) that has 60-90 muscle cells per quadrant and 60-80 cells in the intestine.1,25 The cuticle has three layers. Pseudoterranova spp. have butterfly-shaped lateral chords, and their intestine has a cecum and contains more than 100 intestinal cells.1
While serological testing has been used for diagnosis, particularly in patients with allergic manifestations, it is not standardized and its accuracy remains undemonstrated. There is a high degree of antigenic cross-reactivity between A. simplex and Ascaris suum and Toxocara canis.30
Pathophysiology
Anisakid infection appears to usually be caused by a single worm; however, as many as 56 have been endoscopically extracted from the stomach of a single individual.31 Its ability to burrow through mucosa may be, at least in part, related to its enzymatic production. A. simplex secretes a hyaluronidase with a molecular weight of 40,000 and a pH optimum of 4.0 with no activity at neutral pH.32 It also secretes a metallo-aminopeptidase and a tryspinlike serine protease.1
Infection does not appear to produce protective immunity since repeat episodes may occur.13
Prevention
Since infection of edible fish is common and since the worm may be difficult, if not impossible, to detect (candling is only approximately 70% sensitive in the identification of nematodes in the flesh of fish), the only means of prevention is the avoidance of inadequately prepared fish and shellfish. The FDA states that all fish and shellfish intended for raw or semi-raw (e.g., marinated, partly cooked) consumption should be blast frozen to -35°C (-31°F) or less for 15 hours, or routinely frozen to -20°C (-4°F) or less for seven days.2 Cooking to an internal temperature of 60°C (140°F) for 10 minutes is believed to kill all nematodes and tapeworms. In addition, hard salt curing before pickling is reported to be effective. Anisakis larvae can survive for one day in either soy or Worcestershire sauce, six days in 10% formalin, 51 days in vinegar, and 112 days in 1% HCL.33 Survival is impaired in sake (16% alcohol), but not in wasabe.5
Other Considerations
Infection with other parasites may mimic anisakiasis. Perhaps the nematode most commonly observed in vomitus is Ascaris lumbricoides, but this organism is readily distinguishable by its size (10- 31 cm length in males and 22-35 cm in females). Human infection with the gullet nematode, Gongylonema spp. (e.g., G. pulchrum), results from the inadvertent entry of dung beetles or cockroaches into the oral cavity or their actual ingestion.34,35 While, at 35 mm in the female, this parasite is similar in length to that of A. simplex, it is usually found imbedded within the mucosa or submucosa of the buccal cavity, tongue, or upper esophagus, presenting as an inflammatory mass.
Mammomonogamus laryngeus infection (syngamosis), almost always acquired in the Caribbean islands or in Brazil (infections have also been acquired in Korea, Thailand, and the Philippines), may mimic the "tingling throat" presentation of anisakiasis. The parasite usually infests the respiratory tracts of domestic animals, but may accidentally infect humans. Complaints have included nonproductive cough, a "lump in the throat," a crawling sensation in the throat, hemoptysis, and pneumonitis.36,37
A Korean patient with community-acquired pneumonia was found, on bronschoscopy, to have syngamosis; he recovered after extraction of the parasite and administration of albendazole.15 Thiabendazole and mebendazole have also been used. The male and female of this nematode exist together in copula and can be recognized by the distinctive "Y" shape caused by this union.36 The male is 3-5 mm and the female 9-24 mm in length. Most often, only a single pair is present. The worms are pigmented as a result of hemophagia.
Linguatula serrata, a wormlike blood-sucking parasitic arthropod of the order Pentastomida, the larval form of which is usually found in the nose, frontal sinuses, and tympanic cavity of carnivorous mammals, may cause nasopharyngeal or visceral infection in humans.38 Nasopharyngeal linguatuliasis, also called the Halzoun-Marrara syndrome, results from the ingestion of contaminated raw or undercooked flesh of the herbivorous intermediate host, commonly sheep or goats, and represents a local hypersensitivity reaction to L. serrata nymphs. It may cause sore or itchy throat, congestion, and pharyngeal edema.39 It may also result in unilateral conductive deafness, tinnitus, and facial palsy and may be complicated by otitis media.40 A typical presentation, however, was that of a German tourist in Tunisia who developed cough, hoarseness, dysphagia, anosmia, frontal headache, and epistaxis two hours after ingestion of undercooked meat.41 The diagnosis can be confirmed by detection of the nymphs in nasal discharge. The larval form may migrate and produce disease at other sites, including the eye.42
| Table 3-Worms and Other Stuff in the Mouth |
| Anisakids |
| Ascaris lumbricoides (roundworm) |
| Syngamus laryngeus (gapeworm) |
| Gongylonema pulchrum (gullet worm) |
| Myiasis |
| Midge larva |
| Linguatula serrata (tongueworm) |
| Squid sperm bulbs |
Other causes of wormlike forms in the mouth include oropharyngeal myiasis and infection by the larval form of the chironomid midge.43-45 Each of these is readily recognized as being distinct from anisakids as a result of their size and segmentation; the midge larva reported by Lutwick and colleagues had three thoracic and nine elongated abdominal segments and actively swam with a serpentine motion.
The ingestion of raw squid has been associated with the immediate development of pain and burning in the oral cavity as the result of ejection from numerous spermatophores of sperm bulbs that embed themselves into the mucous membrane. These sperm bulbs grossly appear as 2-3 mm long needlelike structures. The approximately 4 cm long club-shaped spermatophores may be found in the stomach, where they may attach themselves to the gastric mucosa.46
A number of parasitic infestations may mimic the abdominal presentation of anisakiasis. The intestinal form of anisakiasis may be mimicked by infection with Eustrongylides ignotus, which has resulted from ingestion of contaminated sushi or raw minnows.47-49 Eustrongylides infection has been mistaken for acute appendicitis and may cause intestinal perforation.49 The larva is only 80-120 mm by 1-2 mm.
Gnathostomiasis may also cause intestinal lesions; G. doloresi has caused an obstructing colonic mass requiring resection in a man who ate raw snake meat in Japan.50 Angiostrongylus costaricensis, which has occurred after the ingestion of ceviche with contaminated mint, may cause abdominal pathology, including eosinophilic ileitis with perforation.51,52
Enterobius vermicularis may commonly be found in appendices, but its pathologic role in causing appendicitis is uncertain.
References
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2. USFDA Bad Bug Book. Anisakis simplex and related worms. http://vm.cfsan.fda.gov/~mow/chap25.html
3. Oregon State University Service, 1984. http://www. ptialaska.net/~homermap/ parasite.htm
4. Oshima T. Anisakiasis. In: Strickland GT, ed. Hunter’s Tropical Medicine. 7th ed. WB Saunders; 1991: 775-776.
5. Ishikura H, et al. Prog Clin Parasitol 1993;3:43-102.
6. Bhargava D, et al. J Laryngol Otol 1996;110:387-388.
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16. Rushovich AM, et al. Am J Clin Pathol 1983;80: 517-520.
17. Kim LS, et al. Kisaengchunghak Chapchi 1991;29: 93-96.
18. Kark AE, McAlpine JC. Br J Clin Pract 1994;48: 216-217.
19. Ohta M, et al. Am J Gastroenterol 1995;90:1902-1903.
20. Moreno-Ancillo A, et al. Ann Allergy Asthma Immunol 1997;79:246-250.
21. Daschner A, et al. Br J Dermatol 1998;139:822-828.
22. Gomez B, et al. Allergy 1998;53:1148-1154.
23. Fernandez de Corres L, et al. J Investig Allergol Clin Immunol 1996;6:315-319.
24. Muraoka A, et al. Dig Dis Sci 1996;41:2362-2365.
25. Bouree P, et al. Comp Immunol Microbiol Infect Dis 1995;18:75-84.
26. Ido K, et al. J Clin Ultrasound 1998;26:125-130.
27. Matsumoto T, et al. Radiology 1992;183:97-99.
28. Shirahama M, et al. Radiology 1992;185:789-793.
29. Minamoto T, et al. Endoscopy 1991;23:50-52.
30. Iglesias R, et al. Parasitol Res 1997;83:755-761.
31. Kagei N, Isogaki H. Int J Parasitol 1992;22:251-253.
32. Hotez P, et al. J Infect Dis 1994;170:918-926.
33. Olson AC Jr, et al. Am J Med Technol 1983;49: 111-114.
34. Jelinek T, Loscher T. Trop Med Parasitol 1994;45: 329-340.
35. Illescas-Gomez MP, et al. Am J Trop Med Hyg 1988; 38:363-365.
36. Nosanchuk JS, et al. J Clin Microbiol 1995;33: 998-1000.
37. de Lara T de A, et al. Chest 1993;103:264-265.
38. Lazo RF, et al. Am J Trop Med Hyg 1999;60:405-409.
39. el-Hassan AM, et al. Trans R Soc Trop Med Hyg 1991; 85:309.
40. Yagi H, et al. Acta Trop 1996;62:127-134.
41. Buslau M, et al. Dermatologica 1990;181:327-329.
42. Lang Y, et al. Br J Ophthalmol 1987;71:391-395.
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44. Lutwick LI, et al. Infect Med 1996;13:547-548.
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All cases of anisakiasis identifed to date in North America have been due to:
a. A. simplex or Linguatela serrata.
b. A. simplex or Gongylonema pulchrum.
c. Ascaris lumbricoides or P. decipiens.
d. A. simplex or P. decipiens.
Which of the following is correct?
a. The preferred treatment for gastric anisakiasis is albendazole.
b. The symptoms of gastric anisakiasis usually ensue within an hour of ingestion of infested seafood.
c. Massive eosinophilia is present in most patients with gastric anisakiasis.
d. The dominant symptom of patients with gastric anisakiasis is belching; pain is rare.
Which of the following is correct?
a. Candling (transillumination) has a sensitivity in the detection of nematodes in the flesh of fish of only approximately 70%.
b. The diagnosis of human anisakiasis may be made by the detection of A. simplex or P. decipiens ova in the stool.
c. Serological tests for anisakiasis are highly accurate.
d. Human infection by A. simplex may persist for years.
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