Multistate Outbreak of Listeria monocytogenes Infections Linked to start highlightQueso Frescoend highlight — United States, 2021

Investigation and Results

On February 1, 2021, CDC notified state and federal partners of three listeriosis illnesses from Maryland (two cases) and Connecticut (one case) uploaded to PulseNet within the previous 120 days that were highly related (i.e., within four alleles by whole genome sequencing [WGS]). Specimen collection dates ranged from October 20, 2020, to January 6, 2021. All three patients were hospitalized; no deaths were reported. Patients were aged 45–69 years, and one patient was female. All three patients reported Hispanic ethnicity. State partners interviewed patients or their surrogates using the Listeria Initiative questionnaire for hypothesis generation (4). All three patients reported consuming fresh, start highlightsoft cheesesend highlight before becoming ill; two reported consuming queso fresco, a type of fresh, start highlightsoft cheese.end highlight In this outbreak, a case was defined as an infection in a person with a clinical isolate related within five allele differences by WGS and a specimen collection date from October 20, 2020, to March 17, 2021 (Figure).

Based on food histories from the three index patients, their reported Hispanic ethnicity, and the known association between L. monocytogenes and fresh, start highlightsoft cheeses,end highlight CDC asked the Connecticut Department of Public Health (CDPH) to contact the Connecticut patient for brand information. During re-interview, the patient reported consuming brand A queso fresco. CDC conducted a case-case analysis comparing food exposures for four listeriosis patients included in the outbreak (outbreak cases) with completed Listeria Initiative questionnaires to exposures for listeriosis patients not associated with an outbreak by WGS from the same states as outbreak cases (control cases). An exact odds ratio analysis was conducted using SAS software (version 9.4; SAS Institute). Consumption of start highlightqueso fresco (odds ratio [OR] = 51.2; p = 0.002) and other similar fresh, soft cheeses (OR = 30.4; p<0.001)  end highlig were both statistically significant. This activity was reviewed by CDC and was conducted consistent with applicable federal law and CDC policy.*

A total of 13 L. monocytogenes infections that met the case definition were reported from four states (Connecticut [one], Maryland [five], New York [four], and Virginia [three]). Patients ranged in age from <1 year to 75 years (median = 51 years). All patients reported Hispanic ethnicity; seven were female. Twelve patients were hospitalized; one died. Four patients became ill during pregnancy, resulting in two pregnancy losses and one premature birth; one patient remained pregnant after becoming ill. Among the eleven patients who completed the Listeria Initiative questionnaire, start highlightseven reported consuming queso fresco; eight reported consuming other similar fresh, soft cheeses.end highlight Four patients reported consuming brands of cheeses manufactured by firm A, the firm that produces brand A queso fresco.

The Connecticut Food Protection Program and Maryland Rapid Response Team collected samples of fresh, start highlightsoft cheesesend highlight at stores reported by patients, including brand A queso fresco. Connecticut and Maryland collected and tested 61 fresh, start highlightsoft cheeseend highlight samples; two yielded L. monocytogenes. CDPH identified the outbreak strain of L. monocytogenes in two samples of brand A queso fresco. WGS analysis of isolates from the CDPH samples showed they were closely related to the clinical isolates (0–4 allele differences), suggesting that patients became ill from brand A queso fresco. All 13 clinical isolates and two cheese isolates were related within five allele differences by WGS.

Public Health Response

FDA determined that brand A queso fresco was produced by firm A, located in New Jersey, and initiated an inspection. Firm A produced or handled start highlightqueso fresco and two similar fresh, soft cheeses (requesón and quesillo)end highlight under its own brand name and for private label brands. Firm A agreed to recall brand A queso fresco products with expiration dates from February 26 to March 13, 2021. The initial recall and outbreak investigation were announced on February 19, 2021. Because of cross-contamination concerns, firm A agreed on February 26 to expand the recall to all types of start highlightcheeseend highlight produced or handled in the start highlightfacility.end highlight As a result of this investigation, firm A ceased production, repackaging, and distribution of all products manufactured at the facility.

CDC published seven outbreak notices; FDA posted nine outbreak advisories, two recall notices, and two lists of retail establishments that received recalled product. CDC and FDA communications were available in both English and Spanish. In addition, Connecticut published four public communications. Two patients who became ill after the expanded recall, both with specimen collection dates of March 17, 2021, likely purchased and consumed the queso fresco before the recall given their illness dates and the long incubation period for listeriosis (5).

Discussion

Patients in this outbreak were more likely to consume start highlightqueso fresco and other similar fresh, soft cheesesend highlight compared with patients with sporadic Listeria infections reported from the same states. In listeriosis outbreaks, prompt, epidemiologically directed food sampling plays a key role in identifying the source of illness. Without the rapid identification of L. monocytogenes in firm A’s queso fresco, firm A would not have been identified as the outbreak source as quickly. The public health actions taken within 19 days of cluster identification, firm A’s voluntary recalls, and outbreak notices likely prevented additional illnesses or deaths.

In early 2020, during an unrelated outbreak of listeriosis, Listeria grayi and Listeria innocua, typically nonpathogenic to humans, were found in firm A’s processing areas. The presence of Listeria species in a processing environment indicates that L. monocytogenes could survive in that same environment. FDA issued a warning letter to firm A in 2020 because of violations of Current Good Manufacturing Practice regulations and a lack of hazard analysis and preventive control programs (6).

start highlightQueso fresco and other similar fresh, soft cheesesend highlight made with pasteurized milk continue to constitute a serious risk for listeriosis because cheeses can become contaminated during the production process (after milk pasteurization). High moisture, low salt content, and low acidity support growth of L. monocytogenes in these cheeses during refrigerated storage, thereby increasing the risk for illness (7). A study of U.S. listeriosis outbreaks associated with soft cheeses during 1998–2014 found that soft cheeses made with pasteurized milk are implicated in more outbreaks than soft cheeses made with unpasteurized milk, which might be related to higher consumption of cheese made with pasteurized milk or to public health messages advising persons at higher risk for listeriosis not to eat cheeses made with unpasteurized milk. Among 17 outbreaks linked to soft cheeses during 1998– 2014, eleven were linked to start highlightqueso fresco and other similar fresh, soft cheeses,end highlight three of which included cheeses made with unpasteurized milk. The six outbreaks not linked to start highlightthese cheesesend highlight included sheep’s milk, Middle Eastern-style, Eastern European-style, Italian-style, blue-veined, and soft-ripened cheeses (8).

start highlightQueso fresco and other similar fresh, soft cheeses,end highlight especially those produced in facilities with unhygienic processing conditions, have frequently led to listeriosis outbreaks during the last two decades (8). Rapid food testing by regulatory agencies in response to this outbreak investigation identified the implicated cheese. Public health agencies should establish or improve communications, including new methods for disseminating information to emphasize the risk from eating start highlightqueso fresco and other similar fresh, soft cheeses,end highlight even those made with pasteurized milk, to persons at higher risk for listeriosis, including pregnant persons and their newborns, adults aged ≥65 years, and persons with weakened immune systems.