In 2012 local, state, the CDC and the U.S. Food and Drug Administration (FDA) collaborated in an investigation of a multistate outbreak of Salmonella Bareilly and Salmonella Nchanga infections, which was ultimately shown to be associated with consumption of an imported frozen raw yellow fin tuna product, known as Nakaochi Scrape, from Moon Marine USA Corporation. Nakaochi Scrape is tuna backmeat that is scraped from the bones of tuna and may be used in sushi, sashimi, ceviche, and similar dishes.
Salmonella Bareilly and Salmonella Nchanga are unusual serotypes of Salmonella in the United States. Public health investigators used DNA “fingerprints” of Salmonella bacteria obtained through diagnostic testing with pulsed-field gel electrophoresis, or PFGE, to identify cases of illness that were counted as outbreak associated cases. They used data from PulseNet, the national subtyping network made up of state and local public health laboratories and federal food regulatory laboratories that performs molecular surveillance of foodborne infections.
A total of 425 individuals infected with the outbreak strains of Salmonella Bareilly or Salmonella Nchanga. Four hundred and ten persons infected with the outbreak strain of Salmonella Bareilly were reported from 28 states and the District of Columbia. The number of ill persons infected with the outbreak strain of Salmonella Bareilly identified in each state was as follows: Alabama (5), Arkansas (1), California (8), Colorado (1), Connecticut (11), District of Columbia (3), Florida (1), Georgia (20), Illinois (30) Indiana (1), Kansas (1), Louisiana (6), Massachusetts (36), Maryland (39), Missouri (4), Mississippi (2), Nebraska (2), New Hampshire (2), New Jersey (39), New York (62), North Carolina (12), Pennsylvania (37), Rhode Island (6), South Carolina (5), Tennessee (4), Texas (14), Virginia (33), Vermont (1), and Wisconsin (24).
Fifteen persons infected with the outbreak strain of Salmonella Nchanga were reported from 7 states. The number of ill persons infected with the outbreak strain of Salmonella Nchanga identified in each state was as follows: Georgia (2), Maryland (1), New Jersey (3), New York (6), Texas (1), Virginia (1), and Wisconsin (1).
Illness onset dates ranged from January 1 to July 7, 2012. Ill persons ranged in age from less than 1 year to 86 years, with a median age of 30 years; 60% of patients were female. Among 326 persons with available information, 55 (17%) reported being hospitalized. No deaths were reported.
Interviews of ill persons conducted by states in March and April, 2012 suggested consumption of sushi made with raw tuna as a source of these infections. By April 11, 2012, 43 (81%) of 53 ill persons interviewed with a detailed questionnaire reported eating sushi. This proportion was significantly higher when compared with results from a survey of healthy persons in which 5% reported eating “sushi, sashimi, or ceviche made with raw fish or shellfish” in the 7 days before they were interviewed. Of the 43 ill persons reporting eating sushi, 39 (91%) reported eating a sushi item containing tuna and 36 (84%) reported eating a sushi item containing “spicy tuna.”
Several methods were used to evaluate the association between tuna and illness in this outbreak. On March 29, 2012, a study was launched to estimate the frequency of consumption of tuna and “spicy tuna” among all sushi eaters. Investigators assembled a comparison group from 1) diners who ate at one of the cluster restaurants or grocery stores or 2) a restaurant where a single ill person, who was judged to have a reliable memory, recalled consuming sushi only once in the week before illness. Records were collected on sushi orders that were placed at the same time of day (lunch or dinner) and as close to the date when the ill person ate at the restaurant.
On April 9, 2012, preliminary results of the comparison study using information available from 4 illness clusters at restaurants or grocery stores showed that the proportion of sushi orders that contained tuna as an ingredient averaged 61% (ranging from 43% to 71%). The proportion of sushi orders that contained “spicy tuna” as an ingredient averaged 37% (ranging from 29% to 53%). These data suggested there was an association between illness and consumption of sushi made with tuna, and specifically “spicy tuna.”
State and local public health and regulatory officials worked with the U.S. Food and Drug Administration (FDA) to conduct a traceback investigation of tuna. Investigators visited restaurants and grocery stores associated with ill persons and collected information about the ingredients used in “spicy tuna” recipes. Raw tuna was found to be a common ingredient used to make “spicy tuna” among all 5 restaurant or grocery store clusters for which ingredient information was available. FDA selected 4 of the clusters, which were located in Connecticut, Rhode Island, Texas, and Wisconsin, as the focus of the initial traceback investigation. All 4 establishments received the same imported frozen raw Nakaochi Scrape tuna product from a single tuna processing facility in India, Moon Fishery Pvt Ltd.
On April 13, 2012, Moon Marine USA Corporation (also known as MMI) of Cupertino, California voluntarily recalled 58,828 pounds of a frozen raw yellow fin tuna product, labeled as Nakaochi Scrape AA or AAA. A Seafood HACCP (Hazard Analysis and Critical Control Point) inspection was conducted by FDA April 19–24, 2012 at the Moon Fishery Pvt Ltd. processing facility in Aroor, India. Based on the initial tour of the facility, inspectors identified several seafood HACCP deficiencies, such as lack of controls for histamine at receipt of product, lack of controls for Clostridium botulinum at storage, and several significant sanitation observations of concern. A copy of the inspection observations document is available.
During the investigation, samples of the implicated product were collected for laboratory testing. On April 24, 2012, the Wisconsin Department of Health Services announced that the Department of Agriculture Trade and Consumer Protection laboratory had found Salmonella Bareilly contamination in recalled yellow fin tuna and in a spicy tuna roll made with the recalled tuna.
On April 26, 2012, FDA announced finding the outbreak strain of Salmonella Bareilly from two samples taken from unopened packages of recalled Nakaochi Scrape tuna from Moon Marine USA Corporation. One of the samples also yielded another type of Salmonella with a PFGE pattern indistinguishable from a cluster of Salmonella Nchanga infections. Based on an epidemiological link and results of laboratory testing, CDC combined the Salmonella Bareilly investigation with an ongoing Salmonella Nchanga investigation, and the 2 associated PFGE patterns were grouped together as the “outbreak strains.”
By May 17, 2012, laboratory testing conducted by state public health laboratories in Connecticut, Maryland, Massachusetts, Pennsylvania, South Carolina, and Wisconsin isolated Salmonella from 53 (96%) of 55 samples taken from intact packages of frozen yellow fin tuna scrape from Moon Marine USA Corporation or from sushi prepared with the implicated scrape tuna product. Of the 41 Salmonella isolates for which PFGE results are available, 36 samples yielded the outbreak strain of Salmonella Bareilly, and 12 samples yielded the outbreak strain of Salmonella Nchanga. Seven samples yielded the outbreak strains of both Salmonella Bareilly and Salmonella Nchanga.
On May 10, 2012, Moon Fishery (India) Pvt. Ltd., the manufacturer of the frozen yellow fin tuna Nakaochi Scrape, expanded the voluntary to include its 22-pound boxes of “Tuna Strips”, Product of India, marked as “AA” or “AAA Grade” because the product has the potential to be contaminated with Salmonella. The recall was announced after FDA laboratories isolated the outbreak strain of Salmonella Bareilly from a sample of tuna strips from Moon Fishery (India) Pvt Ltd collected as part of increased surveillance efforts. The shipment in question did not enter into U.S. commerce and no human illnesses were associated with this product.