On April 2, 2012, personnel from the Michigan Department of Agriculture and Rural Development detected Salmonella enterica serotype Infantis in an unopened bag of dry dog fooda collected during routine surveillance of retail samples. The dog food had been produced at a plant in Gaston, SC. The plant, which was 1 of 4 plants owned by the production firm, manufactured > 30 brands of dry food products for dogs, cats, and ferrets under the firm's own brands and brands for other companies. A voluntary recall for the dog food product was issued by the production firm on April 6, 2012. Because of the isolation of Salmonella spp from that dry food product, personnel from the South Carolina Department of Agriculture inspected the plant in Gaston on April 9, 2012.
Molecular subtyping of pathogens plays a critical role in detection and investigation of disease outbreaks. In the United States, isolates of strains of Salmonella spp obtained from clinically affected humans are routinely forwarded to state public health laboratories for serotyping and PFGE. The PFGE subtyping patterns are then electronically submitted to PulseNet, the national molecular subtyping network for foodborne disease surveillance.1,2 Several other countries, including Canada, have similar surveillance networks. The PFGE patterns of some nonhuman isolates (eg, isolates obtained from food, domestic animals, and the environment), which are typically collected as a part of routine surveillance, are also uploaded to PulseNet. Therefore, the PFGE pattern of the Salmonella isolate for the dog food was submitted to PulseNet.
The PFGE pattern was uncommon. On April 10, 2012, the PulseNet database was searched for recent human infections of Salmonella Infantis with a PFGE pattern indistinguishable from the isolate found in the dog food sample. A human case was initially defined as an illness in a person with an onset after January 1, 2012, for which culture results yielded Salmonella Infantis with PFGE XbaI pattern JFXX01.0164. That search identified 8 human cases from 6 states reported between February 1 and April 10, 2012. This appeared to be an excessively large number of human cases for that isolate during that time span because typically only 0 to 3 human clinical isolates with that PFGE pattern were uploaded to PulseNet each month. Therefore, a multistate outbreak investigation coordinated by the CDC was initiated on April 10, 2012, to determine the source of the illnesses in humans attributable to that strain and to prevent additional illnesses.
On April 11, 2012, personnel at the plant were informed that there were humans with salmonellosis caused by the same strain of Salmonella spp that had been found in the contaminated pet food product. The plant stopped production of pet foods that evening, and the plant was thoroughly cleaned and disinfected. During April 12 to 20, personnel from the South Carolina Department of Agriculture and the US FDA inspected the plant and collected environmental, ingredient, and finished product samples. Environmental samples were collected from various production (eg, preparation lines and extrusion lines) and nonproduction (eg, carts and floors) surfaces in the plant. Samples were not obtained from plant workers because they were not considered a likely source of contamination. The outbreak strain of Salmonella Infantis was isolated from samples of a finished product, but environmental and ingredient samples collected during this inspection yielded negative results for Salmonella spp. Deficiencies detected during the inspection included lack of assurance (eg, microbial analysis) that pathogens were not introduced into the production line and failure to maintain equipment to protect against contamination or to facilitate cleaning.3 The ultimate source of the contamination and the events leading to the contamination were not determined. The plant resumed production of pet foods on April 18, 2012. On the basis of inspection observations, recommendations were made to increase product testing for detection of contamination with Salmonella spp and address facility protective measures to prevent contamination.
The multistate outbreak investigation of salmonellosis in humans initiated on April 10, 2012, involved personnel from state and local health departments who conducted interviews of case patients using routine enteric disease questionnaires that contained questions about foods, restaurants, travel, and animal contact during the week before each case patient's illness began. Within a few days after initiation of the investigation, additional human cases were identified through PulseNet. Information obtained during interviews with 9 case patients revealed that 6 had contact with a dog in the week before they became ill.
Because of the high rate of exposure to dogs reported in initial interviews, combined with the Salmonella isolate from the retail sample of dry dog food in Michigan, it was hypothesized that these human cases could have been associated with dry pet food manufactured at the production plant in Gaston, SC, where the bag of dog food that yielded the initial Salmonella isolate was produced. The CDC requested that state and local officials reinterview case patients using a CDC questionnaire focused on various pet and pet food exposures. Of 5 case patients who initially remembered the type of dog food with which they had contact, 4 identified 4 brands of dry dog food that had been produced at the Gaston plant. Two case patients provided production code information from packages of 2 dog food products that they had purchased. Those production codes yielded information on the production date, plant, and production line. This information indicated that the 2 products were manufactured at the Gaston plant. On the basis of this information, it was determined that the outbreak of salmonellosis was most likely attributable to the pet food produced at the plant in Gaston.
On April 20, 2012, public health and agriculture officials in Ohio isolated the outbreak strain of Salmonella Infantis from a sample of dry dog food collected at the home of a case patient. The package that contained the dog food was not available, but the case patient indicated the food was a brand produced at the Gaston plant. Subsequently, the outbreak strain was isolated from an unopened bag of the same brand of dry dog food manufactured at the Gaston plant; the bag was obtained from a retail store. A sample of another product collected by the US FDA during an inspection at the Gaston plant on April 30, 2013, also yielded the Salmonella strain involved in the outbreak.
On April 26, 2012, the FDA Coordinated Outbreak and Response Evaluation Network began coordinating regulatory activities. Information collected from case patients and results of product testing were reviewed. Consumer complaints submitted through the FDA consumer complaint system4 were also examined for information about product exposure, production codes, and animals with clinical signs (eg, diarrhea, vomiting, and fever) suggestive of salmonellosis. Production codes from dry dog food linked to human cases and animal illnesses were traced back to pet food produced between late December 2011 and early April 2012 on 2 production lines at the Gaston plant. A voluntary recall was issued on April 26, 2012, for the product from which the outbreak strain was detected in the opened and unopened bags in Ohio.5,6 Another voluntarily recall was issued on April 30, 2012, for the product from which the outbreak strain was detected in the sample collected at the Gaston plant.5,6 Because of investigation findings and growing public health concerns, a recall expansion was issued by the production firm on May 4, 2012, that included all dry food products for dogs and cats that had been manufactured on the 2 implicated production lines between late December 2011 and early April 2012. Other companies opted for inclusion in the voluntary recall expansion or issued individual recalls. These voluntary recalls were issued from May 4 to 8, 2012.6
The recalled products included 16 brands of dry foods for dogs and cats manufactured on the implicated production lines between December 9, 2011, and April 7, 2012. Although no confirmed human illness linked to contaminated cat food was reported, dry food for cats manufactured on the same production lines was recalled out of an abundance of caution. The recalled products had been shipped to 40 states and 26 countries, including Canada, and involved > 27,000 metric tons (> 30,000 tons) of dry foods for dogs and cats.
As more dog food samples were tested, Salmonella Infantis with a second PFGE pattern (XbaI JFXX01.0070), which was also uncommonly reported to PulseNet, was isolated from retail samples of dry dog food produced at the Gaston plant. The case definition was revised to include the second PFGE pattern and to include humans with an illness between January 1 and July 5, 2012, for which culture results yielded Salmonella Infantis with either of the PFGE patterns.
The expanded case definition helped in the identification of additional human cases. Ultimately, the investigation identified 53 individuals from 21 states (n = 51) and Canada (2) who met the case definition (Figures 1 and 2). Eighteen (34%) human cases had the second PFGE pattern. The median age of case patients was 19.5 years (range, < 1 to 82 years); 20 (38%) were children < 2 years of age, and 30 (57%) were female. Of 37 case patients for whom information was available, 12 (32%) were hospitalized; none of the 37 died. Regardless of whether they owned a dog, 28 (76%) reported contact with a dog (in the home or at another location) during the week before the case patients became ill. Of the 21 case patients who remembered the dog food brand, 12 (57%) reported a brand produced at the Gaston plant.
Follow-up inspection by personnel from the US FDA and South Carolina Department of Agriculture during September 10 to 19, 2012, revealed violations similar to those detected during the inspection performed in April 2012. Recommendations for corrective action were provided, and compliance with those recommendations was to be reevaluated during future inspections. Multiple Salmonella strains, but not the outbreak strain, were isolated from environmental samples. No outbreaks of salmonellosis in humans attributable to the strains isolated during the September inspection were identified.
Personnel at the US FDA and state agencies continued analysis of consumer complaints and surveillance of retail samples to determine whether additional recalls or expansion of existing recalls might be required. No additional reports of Salmonella spp isolated from people, pets, or dry pet food manufactured at the Gaston plant had been received from public health and agricultural departments, the FDA consumer complaints system, or other sources as of December 10, 2013.
To identify any illness in pets associated with this outbreak, case patients were interviewed, fecal samples collected from dogs and cats that lived with case patients were tested, and the FDA consumer complaint system was monitored. Of 14 case patients who reported the illness status of their pets, 3 reported that at least 1 dog or cat had been ill.
A number of state and provincial health departments, provincial animal health laboratories, and the FDA Vet-LIRN,7 which is a network of collaborating veterinary diagnostic laboratories, offered to test samples obtained from dogs and cats that resided in households of case patients, with no cost to the owners or attending veterinarians. To our knowledge, animals living in the households of only 4 case patients (2 in the United States and 2 in Canada) were tested (Figure 3).
Two dogs from one of the US households developed diarrhea (loose or runny feces) in March 2012 on approximately the same day as the onset of diarrheal illness in the case patient, a 5-month-old infant. The family was notified about the outbreak in early May 2012. Samples were collected from the household, and the outbreak strain was isolated from the feces of both dogs and from samples collected from an open bag of a brand of dry dog food manufactured at the Gaston plant. The condition of one of these dogs, a 12-year-old dog that was receiving treatment for cancer of the urinary bladder, deteriorated, and the dog was euthanized. The other dog recovered from the episode of diarrhea; follow-up testing of that dog in September 2012 did not yield Salmonella spp.
The other US household had 2 dogs with vomiting, lethargy, fever, and bloody diarrhea during March 2012. Both dogs had consumed a brand of dry dog food manufactured at the Gaston plant. There was improvement in the clinical signs when the dogs were fed a different dog food in early April 2012, and both dogs subsequently had complete resolution of clinical signs. The owners discarded the dry food that may have been produced at the Gaston plant. In early July 2012, approximately 3 months after the illness in the dogs resolved, an infection attributable to the outbreak strain of Salmonella Infantis was diagnosed in the owner's 10-day-old infant. The mother of the infant reportedly had diarrhea 1 day before onset of illness in the infant. The outbreak strain was isolated from fecal samples collected from both dogs a few days after the infant's illness as well as 2 weeks later while the dogs were receiving a 2-week course of ampicillin. In August 2012, a 1-month course of ampicillin was prescribed for both dogs, and fecal samples collected from the dogs in September, October, and December 2012 did not yield Salmonella spp.
One of the Canadian households had 2 dogs and 2 cats. The owners reportedly fed a brand of dry food for dogs and cats manufactured at the Gaston plant. The case patient was a 1-year-old child with illness onset in January 2012. The animals reportedly had vomiting in January 2012 and occasionally had soft feces from January to May 2012; however, Salmonella spp were not isolated from fecal specimens collected from 2 dogs and 1 cat in May 2012. The pet food that had been fed in January was not available in May; however, a sample of the same brand of pet food was collected from the household in May but did not yield Salmonella spp.
The case patient in the other household in Canada was an adult with illness onset in April 2012. The dog in that household was fed dry food manufactured at the plant in Gaston, but the dog had no signs of illness. A fecal specimen obtained from the dog and a sample of the dry food collected from the household in May 2012 did not yield Salmonella spp.
Additional surveillance for animal illnesses linked to the outbreak was performed. In the United States, the FDA consumer complaint system was reviewed for reports of illnesses in animals. An animal case was defined as a gastrointestinal illness (vomiting or diarrhea) in an animal that consumed recalled pet food products that was reported to the FDA consumer complaint system between December 1, 2011, and June 30, 2012. Recall of pet food products was determined on the basis of the production code on the packaging included in the reports. During the period from December 2011 to March 2012, only 1 complaint of a product manufactured at the implicated plant was submitted, but the signs of illness in that animal were not consistent with salmonellosis. During the period from April to June 2012, 167 consumer complaints on brands of products manufactured at the Gaston plant were reported, of which 113 had incomplete or missing production codes and were excluded from further analysis. Of the remaining 54 consumer complaints about products manufactured at the plant, 31 (57%) matched the case definition; those complaints involved 7 brands of recalled product. All 31 cases were illnesses in dogs. Date of illness onset ranged from March 26 to May 7, 2012. Vomiting was reported for 22 (71%) dogs, and diarrhea was reported for 30 (97%) dogs (diarrhea was bloody in 13/30 dogs). The geographic distribution and reported dates of illness onset of these canine cases were similar to those for the human cases (Figures 1 and 2). No illness in cats was linked to recalled products. Follow-up efforts (including testing of fecal and food specimens) were focused on reports of animal illness associated with products manufactured at the Gaston plant outside the recall period as well as products manufactured at other facilities. No additional outbreak-related cases of salmonellosis in animals were identified.
Pulsed-field gel electrophoresis
Veterinary Laboratory Investigation and Response Network
Diamond Pet Foods, Meta, Mo.
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