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Salmonella Reading Illness Outbreak Associated with Turkey, 2017–2019

After-Action Review Report 2018-05

October 14, 2020

The purpose of this report is to share lessons learned from the outbreak with industry and public health partners to help prevent illness and

improve response.

Overview

During December 2017–May 2019, public health officials in multiple states, the Centers for Disease Control and Prevention (CDC), the Food

and Drug Administration (FDA), the Food Safety and Inspection Service (FSIS), the Animal and Plant Health Inspection Service (APHIS), and

the National Turkey Federation (NTF) investigated an outbreak of 356 reported Salmonella Reading illnesses associated with turkey. The

outbreak was linked to human and pet food products that contained turkey, as well as to turkey production and processing environments. One

death was reported from California. The outbreak strain of S. Reading was isolated from a variety of turkey products and from live turkeys. In

contrast to many other foodborne outbreaks that are associated with a specific brand or source of product, evidence suggested that this

outbreak was linked to multiple producers of turkey products and that the outbreak strain was spread throughout the turkey industry. The

investigation spurred two voluntary recalls of FSIS-regulated turkey products (for human consumption) and three voluntary recalls of FDAregulated turkey pet food, though these recalled products did not account for all of the reported human illnesses in this outbreak. This

outbreak response, in which government and industry worked together toward their shared goal to protect consumers, has been used as a

model for government-industry collaboration in subsequent outbreak investigations. In response to this outbreak, NTF published

best practices for reducing Salmonella in turkeys and turkey products.

Epidemiology

During this investigation, investigators used pulsed-field gel electrophoresis (PFGE) and whole genome sequencing, which are both

molecular subtyping techniques, to assess the relatedness of S. Reading isolates and identify the outbreak strain.

On December 19, 2017, FSIS began monitoring a cluster of S. Reading infections in four people, all of whom reported contact with

turkey products prior to illness. Bacterial isolates from these people were indistinguishable by PFGE from each other and from S.

Reading found in eight FSIS turkey samples collected from multiple FSIS-regulated establishments. In January 2018, multiple states,

CDC, and FSIS started investigating the cluster.

Additional people infected with the outbreak strain of S. Reading were reported (356 total cases; see Table 1 for epidemiologic details).

Officials investigated subclusters of ill people to determine factors that may have contributed to illness. Two subclusters in

Minnesota were associated with raw turkey pet food. Two other subclusters, one each in the District of Columbia and Iowa, were

linked to events where a variety of foods, including turkey, were served.

Among 198 ill people with available exposure information, 132 (67%) reported direct or indirect contact with turkey in the week before

illness; 123 prepared or consumed various turkey products that had been purchased raw, 4 lived in homes where pets consumed raw

ground turkey pet food, and 5 worked or lived with someone who worked in a turkey production or processing facility.

No common brand or type was identified among the turkey products that ill people reported consuming.

Public health partners in Canada concurrently investigated poultry-associated illnesses in people from which the outbreak strain of S.

Reading had been isolated.

Since the close of the outbreak investigation, additional human infections with the outbreak strain of S. Reading have been reported,

though at a lower frequency than during the outbreak period.

Table 1. Case characteristics—Salmonella Reading illness outbreak associated with turkey, 2017–2019 (as of March 31, 2019).
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Total number of cases and states of residence 356 cases from 42 states and the District of Columbia (see

CDC map of reported cases )

Illness onset (known or estimated) date range

November 20, 2017–March 31, 2019 (see

CDC timeline of reported cases )

Age range (median) in years

<1–101 (42)

Percent female

48

Number of reported hospitalizations

132

Number of reported deaths

1 (California resident)

Traceback

Investigators conducted traceback investigations for products to which ill people reported exposure. Numerous product brands, types,

and manufacturers were reported; a single, common source was not identified.

Product Sampling

Turkey Products for Human Consumption

The outbreak strain of S. Reading was isolated from 178 samples of raw turkey products from 38 FSIS-regulated establishments

collected via routine FSIS sampling during November 2017–March 2019.

Michigan officials collected two samples of raw turkey products in unopened packaging and three in opened packaging from ill people’s

homes; the outbreak strain of S. Reading was isolated from one unopened package and one opened package.

Arizona officials isolated the outbreak strain of S. Reading from a sample of a raw turkey product in unopened packaging collected from

an ill person’s home.

Per its Policy on Use of Results from Non-FSIS Laboratories (FSIS Directive 10,000.1), FSIS assessed and accepted the above results

from Michigan and Arizona.

Turkey Pet Food

Minnesota officials collected seven samples of raw turkey pet food from ill people’s homes; five of these samples—produced by two

different manufacturers—were positive for the outbreak strain of S. Reading.

FDA officials collected and tested raw turkey pet food in response to a consumer complaint; S. Reading was isolated from this sample,

but not the outbreak strain.

Live Turkeys

APHIS reported that the outbreak strain of S. Reading was isolated from 10 samples from live turkeys in 5 states; these samples had not

been collected as part of this investigation.

Pets

Minnesota officials tested six pet dogs and one pet cat as part of investigations of illnesses associated with raw turkey pet food. Of

these, one dog tested positive for the outbreak strain of S. Reading and three other dogs and the cat tested positive for strains of

Salmonella not related to the outbreak. According to their owners, none of the tested pets had shown signs of illness.

FDA officials tested six pet dogs as part of raw turkey pet food investigations; one dog, which did not appear to be ill, tested positive for

Salmonella (a strain not related to the outbreak) after having been fed raw turkey pet food that tested positive for the outbreak strain of S.

Reading.

Environmental Assessment

Minnesota officials investigated two subclusters of illnesses associated with raw ground turkey pet food and found that ill people may

have been exposed to the outbreak strain of S. Reading by contact with contaminated food, the container in which it was served, or with

the household’s pet dog after it had consumed the contaminated food.
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District of Columbia and Iowa officials assessed turkey preparation practices related to the illness subclusters and found that improper

cooking or handling were likely contributing factors.

NTF worked with government and industry partners to assess factors that may have contributed to the outbreak and the widespread

presence of the outbreak strain in the turkey industry, but was not able to determine the ultimate source of the pathogen or explanation

for its spread.

Industry, Public Health, and Regulatory Actions

FSIS announced on July 19, 2018 that it was monitoring this outbreak.

Isolation of S. Reading from product samples triggered five voluntary recalls, two of FSIS-regulated raw, ground turkey products for

human consumption (November 15, 2018 and December 21, 2018) and three of FDA-regulated raw turkey pet food (February 5, 2018

; January 28, 2019 ; and March 26, 2019 ); however, given the diversity of the types of turkey exposure noted among ill people,

these products did not account for all of the illnesses in this outbreak.

CDC published an Investigation Notice about this outbreak investigation on July 19, 2018 (updated November 8, 2018; November 16,

2018; December 21, 2018; February 15, 2019; final update April 30, 2019).

CDC published a Morbidity and Mortality Weekly Report (MMWR) article about this outbreak investigation on November 22, 2019.

Lessons Learned and Related Policy Actions

Proper Cooking and Handling of Turkey Products

Investigations of illness subclusters linked to human and pet food showed that improper cooking and handling of turkey products likely

contributed to this outbreak. Food preparers should follow these four food safety steps: clean, separate, cook, and chill . Adequate

handwashing is essential after handling raw poultry or after touching pets, their food, or their waste. Turkey products should be cooked

to a safe minimum internal temperature of 165°F as measured by a food thermometer before consumption.

One Health in Action: Collaborating to Respond to a Unique Outbreak

The One Health concept acknowledges the link between the health of people, animals, and their shared environment, as well as the

need for diverse partners from multiple sectors to collaborate to solve health challenges. This complex outbreak and its multi-sectoral

response exemplified One Health, as follows:

Humans, Animals, and the Environment

People and pets were exposed to the pathogen through a variety of turkey products. The turkey production and processing

environments likely were also sources of infection. Persistent epidemiologic evidence and sampling results from turkey products and live

turkeys indicated that the outbreak strain was widespread in the turkey industry.

Novel Response and Surveillance Tools

Unlike many other foodborne outbreaks that are associated with a specific brand or source of product, this outbreak was linked to many

types of raw turkey products. This unique outbreak situation prompted changes in public communication and outbreak surveillance.

For the first time, CDC employed a new public communication tool called the Investigation Notice . This tool is used when an

investigation is either in its early stages and a food item has not been identified, or when an outbreak is linked to a general food

category but not to a specific brand. The tool has been used by CDC in subsequent investigations.

Based on this and other outbreaks, agencies involved in foodborne illness investigations are exploring ways to track pathogen

strains that persistently cause illness for which a specific food vehicle has not been identified.

Collaboration between Government and Industry Partners

Most foodborne outbreaks feature a single food vehicle regulated either by FDA or by FSIS. In contrast, this outbreak was associated

with turkey products regulated by both FDA (turkey pet food) and FSIS (turkey products for human consumption). Effective collaboration

between agencies at all levels of government helped partners detect and respond to this cross-jurisdictional outbreak.

Given the evidence that the outbreak was related to turkeys and turkey products, and that the strain was widespread in the turkey

industry, FSIS and CDC collaborated with NTF during this investigation. Government and industry share a goal to protect consumers

and, as this investigation demonstrated, can appropriately and effectively collaborate on efforts to prevent foodborne illness. This

outbreak response has been used as a model for government-industry collaboration in subsequent outbreak investigations. In response

to this outbreak, NTF:
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Published a document containing best practices for reducing Salmonella in turkeys and turkey products, including potential

on-farm activities. This document is posted on the NTF website and will be reviewed and updated as needed.

Routinely hosts industry meetings on Salmonella reduction efforts.

Continues to support messaging that promotes the awareness of proper handling and cooking of turkey products.

To reduce the risk associated with raw turkey pet food, recommended that its member companies not sell turkey products to pet

food producers without an intervention that would inactivate Salmonella.

Research, Control, and Monitoring

Academia, government, and industry partners are collaborating to investigate the emergence of this outbreak strain of S. Reading.

Additional research into the emergence, transmission, and control of this S. Reading strain and other pathogens in food animals is

warranted.

FSIS continues to monitor the recovery of S. Reading from turkey samples to detect and respond to any concerning trends.

Research to identify ways to further reduce Salmonella in live turkeys and turkey products is also ongoing.

References/Helpful Links

Recalls of FSIS-regulated raw, ground turkey products for human consumption

Recall 112-2018, November 15, 2018

Recall 124-2018, December 21, 2018

Recalls of FDA-regulated raw turkey pet food

Recall , February 5, 2018

Recall , January 28, 2019

Recall , March 26, 2019

CDC Investigation Notice (final update April 30, 2019 )

CDC MMWR article , November 22, 2019

FSIS Directive 10,000.1, Policy on Use of Results from Non-FSIS Laboratories

FSIS Safe Minimum Internal Temperature Chart

4 Steps to Food Safety (clean, separate, cook, and chill)

NTF Salmonella reduction best practices , November 2018

Research study on the emergence of this S. Reading strain

Canada Public Health Notice (final update February 21, 2020 )

Last Modified Oct 14, 2020