Is it safe to eat sushi? Bowel obstruction related to anisakiasis

APRIL 07, 2008

Samantha K. Roland, AB
Medical Student IV

William B. Keeling, MD
Resident
Department of Surgery

Sivaselvi Gunasekaran, MD
Pathologist
Department of Pathology and Cell Biology

David H. Shapiro, MD
Associate Professor of Surgery
University of South Florida
College of Medicine
Department of Surgery
Division of Trauma Surgery
Tampa General Hospital
Tampa, FL

ABSTRACT
Introduction: Sushi is often prepared using raw fish that has been previously frozen. Improperly prepared sushi puts diners at risk for infection from Anisakis or related nematodes. Most reported cases of anisakiasis have occurred in Spain, Japan, and Scandinavia. With sushi and sashimi consumption now commonplace in the United States, it would not be surprising to see an increase in the number of cases reported in this country.

Results and discussion: The authors report a case of anisakiasis in a 28-year-old woman who presented to the emergency department with abdominal pain, nausea, and persistent vomiting. Her symptoms originated shortly after eating sushi 2 weeks earlier. During laparotomy, several granular nodularities were removed from the mesentery of the small bowel and found to contain Anisakis bodies. The authors discuss the life-cycle of the Anisakis parasite and the symptoms and treatment of infected patients, as well as provide an overview of the literature.

Conclusion: Although infection with Anisakis is rare in the United States, surgeons should consider anisakiasis in the differential diagnosis of patients who have eaten sushi or raw fish in the recent past and present with acute gastroallergic symptoms, abdominal pain, or obstruction. Medical treatment for anisakiasis has not been established, and the current recommendation is surgical or endoscopic removal of the parasite.



Anisakis simplex and other related nematodes are known to infect humans who ingest raw or undercooked fish. This includes many types of sushi and sashimi, as well as raw, salted, or pickled herring and anchovies. Although anisakiasis is rarely reported in the United States, sushi bars abound in every American city, and anisakiasis may become a more common cause of abdominal pain and obstruction. Our case is the only one reported in the United States since 2003 where an Anisakis infection resulted in proximal small bowel obstruction.1 We review the literature and discuss the pathophysiology and biology of Anisakis.

 
 

CASE REPORT

A 28-year-old afebrile Asian woman presented to the emergency department reporting a 5-day history of abdominal pain, nausea, and emesis. She had experienced similar symptoms 2 weeks earlier shortly after consuming a sushi dinner, although the symptoms resolved the following morning. The patient had no other gastrointestinal concerns during the intervening 10 days, after which she experienced onset of her current symptoms. She described her abdominal pain as diffuse and her nausea and vomiting as continuous. A physical examination revealed moderate abdominal distention and minimal nonlocalized tenderness to palpation. Her vital signs included a blood pressure of 129/86 mm Hg, heart rate of 98 beats per minute, and a respiratory rate of 16 breaths per minute. Laboratory findings, including a complete blood count, serum chemistries, and urinalysis, were all within normal limits. Radiographs of the patient's abdomen while supine and upright revealed a distended proximal small bowel with air-fluid levels. A computed tomography (CT) scan of the abdomen and pelvis showed proximal small bowel and gastric distention with a transition zone at the proximal jejunum (Figure 1). There was also dilatation of the stomach and duodenum, but no distention of the remaining bowel was observed.

 
 

The patient underwent nasogastric decompression and parenteral fluid resuscitation before undergoing laparotomy, which took place within 12 hours of her presentation. During laparotomy, a nodular band was observed emerging from the base of the mesentery, trapping the bowel and causing obstruction of the jejunum (Figure 2). The odd-looking adhesive band was removed and sent to pathology for evaluation. Several nodules, which were somewhat granular, were removed from the mesentery of the small bowel and sent for examination to the Department of Infections and Parasitic Diseases at the Armed Forces Institute of Pathology. Diagnosis was consistent with Anisakis bodies encased in a granulomatous reaction (Figure 3), and immunoglobulin E (IgE) serology was positive in the convalescent phase for Anisakis. The patient had a benign postoperative course, and her recovery was uncomplicated, except for a superficial wound infection that responded to standard care.

 
 

DISCUSSION

A simplex (also known as the herring worm) is a marine nematode that can be transmitted to humans through consumption of raw or undercooked fish. In a study by Weir, eating raw anchovies and sardines or undercooked hake conveyed the highest risk of transmitting Anisakis infection among Canadians.2 In the United States, the fish most likely to be infected include cod, mackerel, and salmon found just off the California coast and herring from Oregon rivers.3,4 A literature search identified 150 cases of anisakid infection in humans since 2003. The majority of cases occurred in Spain, Japan, and Scandinavia, where the consumption of raw fish is common. Two US cases have been reported in the literature. One involved a patient who experienced a course similar to our patient's.1 The other concerned a patient who had several episodes of cramping over the course of a month and presented to the emergency department after waking up with severe periumbilical abdominal pain.5 He underwent ileocecectomy, and microscopic examination revealed an Anisakis nematode that was "encased in calcified connective tissue infiltrated by eosinophils."5 According to the Division of Parasitic Diseases at the Centers for Disease Control and Prevention (CDC), fewer than 10 cases of anisakiasis are reported in the United States each year.6 Although infection with A simplex is uncommon in this country, frequent consumption of sushi and sashimi puts diners at higher risk of contracting this parasite.

 
 

Life-cycle of Anisakis

Anisakis larvae mature into their adult form in the mucosa of marine mammals (Figure 4). There, the Anisakis worms lay eggs that are excreted with the mammals' feces into the water. The eggs become embry-onated in the water, and first-stage larvae develop within the eggs. The larvae molt and become second-stage larvae, then hatch. Crustaceans ingest the free-swimming larvae, which develop into third-stage larvae in the new host. The larvae migrate into the muscle tissue of fish and squid that eat the crustaceans and are themselves eaten by predatory fish and marine mammals.

Humans become infected after eating raw or undercooked fish infected with Anisakis larvae. After the diner consumes the infected fish, the anisakid larvae begin to penetrate the gastric and intestinal mucosa within hours, causing the first symptoms of anisakiasis. The larvae migrate from the gastric or bowel lumen to the peritoneal cavity and die shortly thereafter, as a result of the patient's immunological inflammatory response. A band of granulomatous tissue forms, with lymphocytic and eosinophilic infiltrate that contains the now-dead larvae. If the larvae pass into the bowel, the patient may experience a severe eosinophilic granulomatous response between 1 to 2 weeks after Anisakis ingestion and exhibit symptoms similar to those commonly associated with Crohn's disease.6

Diagnosis and treatment

Hours after eating infected seafood, the patient may experience abdominal pain, nausea, and vomiting. On occasion, the 2-cm long larvae may be vomited or coughed up from the stomach.6 Lopez-Serrano and colleagues discussed various gastroallergic manifestations of Anisakis, including urticaria, bronchospasm, an-gioedema, and even anaphylaxis after successive exposures.7 Other allergic responses include rash and dyspnea. Weir stressed the need to consider the diagnosis of anisakiasis in any patient who presents with signs of an allergic reaction in combination with abdominal pain.2

Radiographs may reveal bowel obstruction, which is particularly suspicious in a patient who has no hernia and has never undergone surgery. Other manifestations of an anisakid infestation include ulceration of the gastric mucosa, ileitis and colitis, duodenal obstruction, a mesenteric mass resulting in bowel obstruction, and a duodenal tumor. In June 2006, Mineta and associates reported a case of chronic anisakiasis of the ascending colon that was associated with carcinoma.8 The authors noted that 75 cases of colonic and rectal Anisakis infection have appeared in the Japanese literature.8

Diagnosis can be made during gastroscopic examination, at which time any observed larvae may be removed. Anisakiasis can also be diagnosed by conducting a histopathology examination of tissue taken during biopsy or surgery.6 A suspected diagnosis should be confirmed using IgE serology specific for A simplex. Results will usually be negative for tests conducted within the first 2 weeks after exposure, which was the case with our patient. Two weeks or more following exposure, the IgE test has a sensitivity of 70.4% and specificity of 87.1%.9 This test is available at referral laboratories in the United States, such as the Mayo Clinic laboratory.

Masui and associates report a case similar to ours, involving a patient who experienced entrapment of the terminal ileum by a peritoneal band consisting of granulomatous inflammation and a section of necrotic tissue surrounding an Anisakis larva.10 Tissue eosinophilia around the larvae is typical, but abnormal levels of eosinophils in the peripheral blood is not required to make the diagnosis.

Current recommended treatment of anisakiasis is surgical or endoscopic removal of the larvae.6 In a review of fish-borne parasites in Asia, Nawa and colleagues noted that there is no established medical treatment for Anisakis, but they did cite a few cases in which albendazole (Albenza, Eskazole, Zentel) proved effective.11

CONCLUSION

Sushi restaurants abound in the United States, and raw fish consumption has become increasingly common. Raw fish must be adequately frozen prior to preparing sushi or sashimi to help prevent Anisakis infection. Clinicians should consider anisakiasis in the differential diagnosis of any patient presenting with acute gastroallergic symptoms in conjunction with abdominal pain or obstruction and query such patients about any recent ingestion of sushi, sashimi, or other raw or undercooked fish. Home preparation of sushi using one's own catch is particularly risky, and suspicions should be elevated for patients who acknowledge having eaten sushi prepared from wild-caught fish.

Disclosure

The authors have no relationship with any commercial entity that might represent a conflict of interest with the content of this article and attest that the data meet the requirements for informed consent and for the Institutional Review Boards.


REFERENCES

  1. Schuster R, Petrini JL, Choi R. Anisakiasis of the colon presenting as bowel obstruction. Am Surg. 2003;69(4):350-352.
  2. Weir E. Sushi, nematodes and allergies. CMAJ. 2005;172(3):329.
  3. Sakanari JA, McKerrow JH. Anisakiasis. Clin Microbiol Rev. 1989;2(3):278-284.
  4. Shields BA, Bird P, Liss WJ, et al. The nematode Anisakis simplex in American shad (Alosa sapidissima) in two Oregon rivers. J Parasitol. 2002;88(5):1033-1035.
  5. Chu K, McKerrow JH, Binmoeller KF, et al. Attack of the sushi worm: abdominal pain caused by intestinal anisakiasis. Surg Rounds. 2005;28(4):180-183.
  6. Parasites and health. Centers for Disease Control & Prevention, Division of Parasitic Diseases Website. Available at: www.dpd.cdc.gov/dpdx/html/anisakiasis.htm. Accessed February 4, 2008.
  7. L?pez-Serrano MC, Gomez AA, Daschner A, et al. Gastroallergic anisakiasis: findings in 22 patients. J Gastroenterol Hepatol.2000;15(5):503-506.
  8. Mineta S, Shimanuki K, Sugiura A, et al. Chronic anisakiasis of the ascending colon associated with carcinoma. J Nippon Med Sch.2006;73(3):169-174.
  9. Matsushita M, Okazaki K. Serologic test for the diagnosis of subclinical gastric anisakiasis. Gastrointest Endosc. 2005;61(7):931.
  10. Masui N, Fujima N, Hasegawa T, et al. Small bowel strangulation caused by parasitic peritoneal strand. Pathol Int. 2006;56(6):345-349.
  11. Nawa Y, Hatz C, Blum J. Sushi delights and parasites: the risk of fishborne and foodborne parasitic zoonoses in Asia. Clin Infect Dis.2005;41(9):1297-1303.

Self-assessment questions

  1. An individual can contract anisakiasis:
    1. Only in underdeveloped countries
    2. Eating at sushi restaurants that have substandard sanitary conditions
    3. From eating fresh-caught raw fish
    4. From eating frozen raw fish
  2. What is the most specific way to diagnose Anisakis infection?
    1. Conducting a physical examination
    2. Obtaining a thorough patient history
    3. Taking radiographs
    4. Serology tests
  3. The signs and symptoms of Anisakis infection may include:
    1. Allergic reactions
    2. Abdominal cramping
    3. Nausea and vomiting
    4. All of the above
  4. How many cases of anisakiasis occur in the United States annually?
    1. 10 to 15
    2. Fewer than 10
    3. More than 50
    4. None

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