Multistate Outbreak of Listeriosis Associated With Packaged Leafy Green Salads

United States and Canada, 2015-2016

Julie L. Self; Amanda Conrad; Steven Stroika; Alikeh Jackson; Laura Whitlock; Kelly A. Jackson; Jennifer Beal; Allison Wellman; Marianne K. Fatica; Sally Bidol; Paula Pennell Huth; Meghan Hamel; Kristyn Franklin; Lorelee Tschetter; Christine Kopko; Penelope Kirsch; Matthew E. Wise; Colin Basler


Emerging Infectious Diseases. 2019;25(8):1461-1468. 

In This Article


Investigation in the United States

Epidemiologic Investigation. We identified 19 cases of listeriosis in 9 states: Connecticut (1), Indiana (1), Massachusetts (1), Michigan (4), Montana (2), New Jersey (1), New York (6), Ohio (2), and Pennsylvania (1) (Figure 1). All patient isolates were serotype 4b, indistinguishable by PFGE pattern combination, 7-gene sequence type (ST) 382, and closely related genetically to one another by wgMLST, differing by a median of 3 alleles (range 0–16 alleles).[20] Illness onset dates were July 5, 2015–January 31, 2016 (Figure 2). Of the 8 cases initially detected, 5 were later excluded by using this case definition because the isolates were different by ≥16 alleles and had isolation dates before July 5, 2015.

Figure 1.

Outbreak-related cases of listeriosis (n = 19) in the United States by state of residence, July 5, 2015–January 31, 2016.

Figure 2.

Timeline of Listeria monocytogenes isolation for 19 US patients during outbreak associated with packaged leafy green salads, July 5, 2015–January 31, 2016.

All 19 patients were hospitalized; listeriosis contributed to 1 (5%) death. Case-patients had a median age of 64 (range 3–83) years; 14 (74%) were female. One case of listeriosis in a pregnant woman resulted in a preterm live birth. Meningitis developed in 1 otherwise healthy child with listeriosis (Table 1).

No exposures on the standard LI questionnaire were commonly reported by case-patients in the cluster, and case–case comparisons did not generate any potential food items. Five case-patients completed supplemental interviews, and 12 case-patients completed iterative, open-ended interviews. One patient refused to be reinterviewed but provided a detailed dietary log for analysis. Ultimately, data on leafy green vegetable consumption was available for 16 (84%) of 19 patients; all 16 reported consuming leafy green salads, including 81% (13/16) reporting romaine lettuce and 71% (10/14) reporting spinach. Of those specifically asked, 93% (13 of 14) reported consuming packaged leafy green salads in the 28 days before illness onset. Nine case-patients recalled brand information; 2 packaged leafy green salad brands were reported that we determined came from a single processing facility in the United States (Table 2). Five case-patients were able to provide receipts or shopper card records to confirm purchase dates, locations, and brands. School or residential facility menus and invoices suggested potential exposure to leafy green salads for 2 additional case-patients who could not be interviewed.

Regulatory Investigation. On January 14, 2016, PulseNet staff analyzed sequence data from L. monocytogenes isolated from a packaged leafy green salad that was collected by ODA during routine retail sampling and found that it was closely related by wgMLST to clinical isolates from case-patients (median 3 alleles, range 0–16 alleles). On the basis of these laboratory results, in combination with preliminary epidemiologic data suggesting a link to leafy green salads, on January 16, 2016, FDA initiated an inspection of the facility that processed the packaged leafy green salad.

During the facility inspection, FDA investigators observed factors that might contribute to L. monocytogenes contamination, including failure to collect environmental samples from food contact surfaces, collection of environmental samples only before production, and failure to conduct follow-up investigations beyond the standard practices after identifying Listeria spp. from environmental samples over a period of 19 months.[21] Review of records indicated that the sampling program of the facility had yielded Listeria spp. 11 times during July 21, 2014–January 7, 2016. Finished product, including a Caesar salad kit, and in-line samples of romaine lettuce from a production line collected by FDA from the facility on January 16, 2016, yielded L. monocytogenes (Table 3). Results from the Caesar salad kit were confirmed positive for L. monocytogenes on January 26, 2016, and those for in-line romaine lettuce were confirmed positive for L. monocytogenes on January 28. L. monocytogenes was isolated on February 9, 2016, from an open container of packaged leafy green salad collected from the home of 1 case-patient; the salad had been processed at the same facility in the United States. Five isolates identified from the processing facility and 1 leftover product from the home of a patient were closely related by wgMLST to clinical isolates and the retail isolate (median 3 alleles, range 0–16 alleles).

The inspection findings, the well-documented ability of Listeria species to persist in food processing/manufacturing environments, and the span of clinical cases over a period of months suggested that the source of the contamination was likely the processing/manufacturing environment, rather than a harvest site. As a result, no traceback to source farms was performed. After the FDA inspection, the processing facility implemented corrective actions.

Epidemiologic Investigation in Canada

PHAC identified 14 cases of listeriosis in 5 eastern provinces: Ontario (9), Quebec (2), New Brunswick (1), Prince Edward Island (1), and Newfoundland and Labrador (1). Illness onset dates were May 7, 2015–February 23, 2016. Ten case-patients matched the primary outbreak PFGE pattern, and 4 matched secondary PFGE pattern A. Nine (90%) of 10 isolates from patients in Canada with the primary PFGE pattern were closely related genetically to one another (0–5 SNPs) and would have met the US case definition; 1 patient from Canada with the primary PFGE pattern was not closely related to the others by WGS (>35 SNPs from outbreak cases). Isolates with secondary PFGE pattern A were not closely related genetically to one another and were genetically distinct from isolates with the primary PFGE pattern. All case-patients in Canada were hospitalized, and 3 (21%) died, but it was not determined whether listeriosis contributed to the deaths.

Detailed food exposure information was collected for all 10 case-patients who had the primary outbreak PFGE pattern. Eight (80%) reported consuming packaged leafy green salads and salad kits before illness onset. Brand information was available for 4 case-patients, and all reported or provided a purchase history that included brands made at the same US processing facility. One case-patient with secondary PFGE pattern A was interviewed by using the focused questionnaire and reported consuming coleslaw but was unable to recall the brand or product details.

Regulatory Investigation in Canada

CFIA collected and tested 137 packaged leafy green salads at the retail level, representing 45 unique product type and lot code combinations processed at the same US processing facility during January 3–14, 2016. Packaged leafy green salads from 4 unique product types and lot code combinations yielded L. monocytogenes; these products included 3 varieties of packaged salad (Chopped Romaine, Caesar Salad Kit, and Colorful Coleslaw), 4 production dates (January 9–14, 2016), and 3 production lines (Table 3). Three of these varieties yielded the primary PFGE pattern that was indistinguishable from the US outbreak strain. The isolate from Colorful Coleslaw, which was distributed only in Canada, had secondary PFGE pattern B, which was not closely related by wgMLST to other clinical or food isolates. WGS showed that all food isolates from Canada that had the primary outbreak PFGE pattern were closely related to one another, to the 9 closely related clinical isolates from Canada that had the primary PFGE pattern, and to the US clinical and food isolates (range 0–16 SNPs).[20]

Product Actions and Public Reporting

On the basis of the epidemiologic data and the ODA retail surveillance sample of packaged salad that yielded the outbreak strain of L. monocytogenes, on January 21, 2016, the US processing facility voluntarily stopped production of all packaged leafy green salads because of possible L. monocytogenes contamination. On January 22, the facility issued a market withdrawal of products manufactured at that location, including 22 varieties of packaged salad sold under 6 brands in the United States and 2 brands in Canada, both organic and nonorganic brands. These products were distributed to ≥23 states in the eastern and midwestern United States and eastern regions of Canada.[22,23] CDC, FDA, PHAC, and CFIA issued communications advising the public how to identify affected products by the manufacturing code found on the package and advised consumers and retailers to discard affected products.[22–25] Consumers and retailers were also advised to thoroughly wash and sanitize anything that might have come in contact with the affected products, including refrigerator drawers and shelves, reusable grocery bags, food storage containers, countertops, and food preparation tools.[22,24,26] On January 27, after receiving notification from FDA that samples from packaged leafy green salads collected during the facility inspection were confirmed positive for L. monocytogenes, the firm issued a voluntary recall of all packaged salad products made at the US processing facility with information for consumers to identify the recalled products and brands.[27]