The U.S. Food and Drug Administration conducted an assignment to inspect ice cream production facilities across the country in 2016 and 2017 to determine the prevalence of certain types of harmful bacteria in these establishments and whether they were implementing food safety programs to control pathogens.
The FDA began the assignment on August 1, 2016, following 16 recalls of ice cream products due to the presence of pathogens in the prior three years, and an outbreak of listeriosis linked to an ice cream maker in 2015 that involved three deaths.
The assignment, which entailed both inspections and environmental sampling, was designed to gain insights into the extent to which Listeria monocytogenes and Salmonella spp. contamination may be in the manufacturing environment; to evaluate each establishment’s ability to prevent contamination from environmental pathogens; and to assess whether monitoring procedures and frequencies, sanitation methods, and manufacturing processes at each establishment are sufficient to identify, prevent, reduce, and/or eliminate microbial hazards of public health concern. The assignment did not include testing of finished product for the presence of Listeria monocytogenes and Salmonella.
In targeting Listeria monocytogenes and Salmonella for this assignment, the FDA considered that these pathogens may be present in processing environments or may be introduced through ingredients.
The assignment was not conducted to ensure compliance with the Preventive Controls for Human Food rule established by the FDA Food Safety Modernization Act (FSMA). The FDA began the assignment about a month before larger food facilities were required to comply with the rule, and one to two years before small and very small businesses were required to comply.
However, the findings underscore the need for the development and implementation of a food safety plan as required by the Preventive Controls rule. Establishments covered by the rule, including those that make ice cream, are required to have a written food safety plan, based on an analysis of likely hazards. Listeria monocytogenes and Salmonella are examples of hazards, if identified in a food safety plan, that a company would be required to minimize with preventive controls and verify that their controls are working.
For a year, the FDA conducted inspections and environmental sampling of 89 ice cream production facilities in 32 states . In selecting facilities for inclusion in the assignment, the agency sought to ensure representation from throughout the country and favored larger establishments whose product would be expected to reach greater numbers of consumers. At the time the assignment was conducted, the 89 ice cream production facilities inspected accounted for about 16 percent of the domestic ice cream manufacturers in the FDA’s inventory.
The agency instructed its investigators to collect two environmental samples at each establishment, one consisting of at least 50 subsamples to test for Listeria monocytogenes and the other consisting of at least 100 subsamples to test for Salmonella.
The FDA detected Listeria monocytogenes in 19 of the 89 establishments (an establishment-based prevalence of 21.3%), and in 65 of the 5,295 subsamples (a subsample-based prevalence of 1.25%). Examining the findings by zone, the agency detected Listeria monocytogenes on food contact surfaces at one of the 19 establishments where Listeria monocytogenes had been found, whereas all the other detections of the pathogen involved non-food contact surfaces.
The agency detected Salmonella in one of the 89 ice cream production facilities (an establishment-based prevalence of 1.1%), and in one of the 7,004 subsamples (a subsample-based prevalence of 0.01%). The FDA collected the Salmonella-positive sample from a non-food contact surface, the wheel of a forklift that transported ingredients from a storage area to a production area.
The FDA also conducted whole genome sequencing (WGS) of the subsamples that tested positive for a pathogen to identify the bacteria’s genetic patterns and determine whether the bacteria may be linked to human illness, finished products, or other environmental samples. A subsequent bioinformatics analysis showed that three of the Listeria monocytogenes-positive samples were individually related to isolates obtained from four ill persons prior to 2016. However, at the time of the collection and testing, the FDA could not determine whether any of the bacteria found in the environment of the facilities were the likely cause of those four illnesses, due to the limited epidemiological data then available. In late summer 2018, additional information surfaced, strongly linking a Florida facility inspected under this assignment to a clinical listeriosis case. Working collaboratively, the FDA, Centers for Disease Control and Prevention (CDC), and state health officials determined that the Listeria monocytogenes isolate obtained from the clinical case was highly related to a positive environmental sample collected at the Florida facility in 2017. State health officials confirmed that the patient had eaten ice cream made at the facility, and a follow-up inspection by the FDA identified insanitary conditions that could lead to Listeria monocytogenes contamination in finished product.
Alerted to the link to the clinical listeriosis case, the firm conducted a voluntary recall of all product within expiry. On October 19, 2018, the FDA suspended the firm’s food facility registration, and subsequently the firm voluntarily ceased operations. In the months following the suspension, the firm submitted a proposed shift in business to become a warehouse distributor of ice cream products. The company will not resume ice cream manufacturing operations, but instead will store and distribute product sourced from third party manufacturers. Given the proposed changes and commitments by the firm, along with FDA site inspection and verification, the agency lifted the suspension on February 15, 2019, reinstating the firm’s facility registration.
With respect to the assignment inspectional outcomes, the FDA classified 44 of the 89 inspections (49.4%) as “No Action Indicated (NAI),” meaning no objectionable conditions or practices were observed during the inspection; 39 inspections (43.8%) as “Voluntary Action Indicated (VAI),” meaning objectionable conditions or practices were observed and documented, but the operation should be able to address them without official action by the FDA; and six inspections (6.7%) as “Official Action Indicated (OAI),” meaning objectionable conditions or practices warranting official action by the FDA were observed and documented.
The inspections classified as OAI as compared to VAI were characterized by conditions or practices most likely to contribute to contamination in the food. The FDA detected Listeria monocytogenes in all six of the facilities that received an OAI classification. In addition to the pathogen findings, agency investigators observed, for example, improper cleaning and sanitizing of utensils and production equipment food contact surfaces; employees’ failure to thoroughly wash hands before starting work and after handling trash; a sink with holes that allowed waste water to drip onto the production room floor; and the use of a pressurized hose to spray waste product toward a floor drain while ingredients and food packaging were unprotected from the splash and mist.
The FDA’s regulatory response(s) to the findings at each facility are provided in this table. In addition to the suspension described above, the agency worked with two firms to conduct voluntary recalls, held seven regulatory meetings , and notified management at 39 facilities of the need to take voluntary corrective actions. Also, follow-up inspections are being conducted by the FDA at all the facilities that received an OAI classification. As one example, at the facility where the FDA detected Listeria monocytogenes in 30 percent of the subsamples (establishment No. 3 in the table), agency investigators conducted a follow-up inspection and environmental sampling and did not find environmental pathogens, verifying that the firm took effective corrective action.
The table that follows provides the test results, inspectional outcomes and regulatory follow-up in response to all findings under this assignment.
 The FDA excluded five inspections from the assignment data set because upon review they did not meet the assignment criteria. Three of the five facilities were not making ice cream at the time of the inspection; one made popsicles but not ice cream; and one received, stored and distributed ice cream but had ceased making it.
 The FDA holds a regulatory meeting to inform responsible individuals or firms about how one or more products, practices, processes, or other activities may be in violation of the law. Such a meeting can be effective in obtaining prompt voluntary compliance.