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Published Date: 2017-03-17 13:46:01
Subject: PRO/AH/EDR> Salmonellosis, st Enteritidis - USA: restaurant chain, truffle oil, 2015
Archive Number: 20170317.4906263
A ProMED-mail post
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International Society for Infectious Diseases

Date: Thu 16 Mar 2017
Source: MMWR 2017;66:278-281

Ref: Kuramoto-Crawford SJ, McGee S, Li K, et al: Investigation of _Salmonella_ Enteritidis outbreak associated with truffle oil -- District of Columbia, 2015. MMWR Morb Mortal Wkly Rep 2017;66:278-281. doi: doi: 10.15585/mmwr.mm6610a4
On 8 Sep 2015, the District of Columbia Department of Health (DCDOH) received a call from a person who reported experiencing gastrointestinal illness after eating at a District of Columbia (DC) restaurant with multiple locations throughout the USA (restaurant A). Later the same day, a local emergency department notified DCDOH to report 4 persons with gastrointestinal illness, all of whom had eaten at restaurant A during 30 Aug-5 Sep 2015. 2 patients had laboratory-confirmed _Salmonella_ group D by stool culture. On the evening of 9 Sep 2015, a local newspaper article highlighted a possible outbreak associated with restaurant A. Investigation of the outbreak by DCDOH identified 159 patrons who were residents of 11 states and DC with gastrointestinal illness after eating at restaurant A during 1 Jul-10 Sep 2015. A case-control study was conducted, which suggested truffle oil-containing food items as a possible source of _Salmonella enterica_ serotype Enteritidis infection. Although several violations were noted during the restaurant inspections, the environmental, laboratory, and traceback investigations did not confirm the contamination source. Because of concern about the outbreak, the restaurant's license was suspended during 10-15 Sep 2015. The collaboration and cooperation of the public, media, health care providers, and local, state, and federal public health officials facilitated recognition of this outbreak involving a pathogen commonly implicated in foodborne illness.

Epidemiologic investigation
To identify food items associated with gastrointestinal illness, DCDOH initiated a case-control study; a case was defined as the occurrence of gastrointestinal illness in a person beginning 7 days or less after eating at restaurant A during 1 Jul-10 Sep 2015. Cases were categorized as confirmed (_Salmonella_ group D isolated from a clinical specimen by culture) or probable (linked epidemiologically, but without laboratory confirmation of _Salmonella_). Case-patients were identified on the basis of laboratory reports confirming _Salmonella_, self-report (that is., contacted DCDOH directly), notifications from health care providers, and referrals from other restaurant patrons. Control subjects ate at restaurant A during 1 Jul- 10 Sep 2015, but did not report gastrointestinal illness. Control subjects were identified through case-patients or self-reported to DCDOH. Case-patients and control subjects were interviewed using the DCDOH foodborne investigation questionnaire and were asked to review restaurant A's online menu and list all food items ordered, shared, or tasted. Sociodemographic and clinical information (such as symptoms, doctor visits) was also collected.

During 9 Sep-28 Oct 2015, DCDOH identified 277 patrons who ate at restaurant A, among whom 254 (92 percent) were interviewed directly or through a proxy and included in the analysis. Among the 254 interviewees were 159 (63 percent) case-patients (40 confirmed and 119 probable) and 95 (37 percent) control subjects. The majority (90 percent) of illness onset dates occurred during 31 Aug-10 Sep 2015 (Figure [for figure and tables, see source URL above - Mod.LL]). Case-patients included DC residents and residents of 11 states, many of whom were visiting DC during the Labor Day weekend [5-18 Sep 2015]. No significant differences were noted between case-patients and control subjects in terms of age, sex, race/ethnicity, and place of residence (Table 1). Among the 153 case-patients for whom symptom information was available, 143 (93 percent) reported diarrhea, 128 (84 percent) abdominal cramps, 105 (69 percent) chills, 103 (67 percent) headache, 100 (65 percent) nausea, and 82 (54 percent) fever.

Food items consumed by 155 probable and confirmed case-patients and 88 control subjects were compared. 6 food items were significantly associated with case status (Table 2), 3 of which (beef carpaccio, truffle mushroom croquette, and truffle risotto) contained truffle oil. When all truffle oil-containing items were combined into a single variable, including the 3 that were individually significant, consumption of a truffle oil-containing item was reported by 89 percent of case-patients compared with 57 percent of control subjects (p less than 0.001).

DCDOH interviewed 6 of 7 restaurant A employees who reported illness to their manager from late August through early September [2015], the period when most patron illnesses occurred. 2 employees sought medical care; one submitted a stool sample for laboratory testing and was confirmed to have a _Salmonella_ Enteritidis infection. This employee, who reported eating a truffle oil-containing item that was not offered on the menu in addition to other restaurant A food items, was not involved in food preparation.

Environmental and laboratory investigations
On 9 Sep 2015, a routine restaurant inspection was performed in response to the complaint received the previous day. Although multiple food safety violations were noted, the inspection findings did not warrant restaurant closure. On 10 Sep 2015, a 2nd inspection was conducted as part of the outbreak investigation. Food samples collected on 9 and 10 Sep 2015, and environmental samples collected on 11 Sep 2015 were tested for _Salmonella_. Truffle fries sampled from the deep fryer and uncooked truffle mushroom croquettes were among the samples collected on 10 Sep 2015; a truffle oil sample was collected on 14 Sep 2015. DC Public Health Laboratory (DCPHL) and state public health laboratories performed pulsed-field gel electrophoresis (PFGE) testing on isolates from clinical specimens and uploaded pattern results into PulseNet (1). The outbreak cluster code was assigned using clinical samples from two initial hospitalized patients.

DCPHL tested the truffle fries, which screened positive for _Salmonella_ by using polymerase chain reaction (PCR), but _Salmonella_ was not isolated during confirmatory testing. All other food and environmental samples were negative for _Salmonella_. Among persons who reported illness, 41 (40 patrons and one employee; 26 percent) had stool samples collected. All 41 had the outbreak _Salmonella_ Enteritidis strain (PFGE XbaI pattern JEGX01.0008).

Traceback investigation
DCDOH issued a nationwide call for cases through CDC's Epidemic Information Exchange on 10 Sep 2015. Approximately 1 week later, the Los Angeles County Department of Public Health notified DCDOH of a possible outbreak associated with the same restaurant chain at a Los Angeles restaurant. On 1 Oct 2015, the Food and Drug Administration and the New York State Department of Agriculture and Markets inspected the New York based commissary that prepared and distributed food items to both restaurant locations. Distributed food items to both restaurants were similar and included truffle oil, dried mushrooms, and croquette mix. Food items were unavailable for testing because the commissary had voluntarily ceased operations on 13 Sep 2015. Analysis of 102 subsamples of environmental sponges from food preparation areas using the VIDAS Enzyme Linked Fluorescent Assay did not detect _Salmonella_ species. Shipment records for black trumpet mushrooms, cremini mushrooms, truffle oil, and food items prepared at the commissary using these ingredients were reviewed. The records for the implicated truffle oil shipped during 1 Aug-15 Sep 2015 yielded no significant findings. Truffle oil was regularly shipped to all restaurant A locations across the United States, including locations without any reported illnesses.

Public health response
DCDOH issued a summary suspension of restaurant A's license on 10 Sep 2015 because of increasing concern about a potential outbreak. Restaurant A removed truffle oil-containing food items from the menu and was required to address food safety risk factor violations before its license was restored. After reopening on 16 Sep 2015, restaurant A was required to undergo periodic inspections. No additional _Salmonella_ Enteritidis cases have been reported since restaurant A reopened.

Gastrointestinal illness was reported in 159 persons from 11 states and DC after eating at restaurant A during July-September 2015. All confirmed _Salmonella_ Enteritidis cases had indistinguishable PFGE patterns. The case-control study results indicated truffle oil as a likely source of infection. Approximately 90 percent of case-patients reported that they ate a truffle oil-containing item.

Although _S._ Enteritidis is most commonly associated with poultry and eggs (2,3), the strain identified in this outbreak was also associated with consuming Turkish pine nuts in a 2011 multistate outbreak (4). Whole genome sequencing conducted by CDC identified significant differences between this strain and the one implicated in the 2011 pine nut outbreak. Previous reports indicate that _S._ Enteritidis has the capacity to thrive in low-water activity foods (such as nuts and oils) (5), including peanut oil (6).

The findings in this report are subject to at least 3 limitations. First, attributing an outbreak to a single food vehicle is a recognized challenge in foodborne outbreak investigations (2). In this situation, food and environmental samples were collected after restaurant A had begun disposing of food items and addressing potential sources of contamination, and the commissary inspection occurred after its closure. Second, the truffle oil sampled on 14 Sep 2015 was unlikely to have been consumed by case-patients, because the latest meal date for case-patients was 9 Sep 2015. Finally, because of failure to isolate the organism in culture from food samples, it could not be established whether the PCR-detected _Salmonella_ in the truffle fries led to actual illness or matched the outbreak strain. Despite these limitations, the epidemiologic evidence strongly suggested that truffle oil was the likely source of the outbreak.

Recognition of this multistate outbreak associated with truffle oil might have easily gone unnoticed; restaurant patrons and emergency department staff played a significant role in its timely recognition. The PFGE pattern associated with this outbreak is the eighth most common in the PulseNet database. Assigning a specific cluster code for this suspected outbreak at the time isolates from the hospitalized cases were added to PulseNet was difficult because uploads for the pattern code had not exceeded normal thresholds. Close collaboration between DCDOH epidemiologists and DCPHL ultimately led to a cluster code assignment, which facilitated case identification in residents of other states. Results from the routine inspection conducted after the initial complaint did not alone warrant restaurant closure; however, increasing concern about a potential outbreak, based on multiple complaints of illness, prompted DCDOH to suspend the restaurant's license a day later. This timely public health response likely prevented additional illnesses, because 9 percent of case-patients reported eating at restaurant A the day before the closure. The engagement of the public, media, health care providers, and local, state, and federal public health officials facilitated recognition of an outbreak involving a _Salmonella_ serotype that is a common source of foodborne illness.

1. Gerner-Smidt P, Hise K, Kincaid J, et al: Pulsenet Taskforce. PulseNet USA: a five-year update. Foodborne Pathog Dis 2006; 3(1): 9-19; abstract available at
2. Jackson BR, Griffin PM, Cole D, Walsh KA, Chai SJ: Outbreak-associated _Salmonella_ enterica serotypes and food commodities, United States, 1998-2008. Emerg Infect Dis 2013; 19(8): 1239-44; available at
3. Chai SJ, White PL, Lathrop SL, et al: _Salmonella_ enterica serotype Enteritidis: increasing incidence of domestically acquired infections. Clin Infect Dis 2012; 54(Suppl 5): S488-97; abstract available at
4. CDC. Multistate outbreak of human _Salmonella_ Enteritidis infections linked to Turkish pine nuts (final update). Atlanta, GA: US Department of Health and Human Services, CDC; 2011; available at
5. Finn S, Condell O, McClure P, et al: Mechanisms of survival, responses and sources of _Salmonella_ in low-moisture environments. Front Microbiol 2013; 4:331; available at
6. Fong K, Wang S. Strain-specific survival of _Salmonella_ enterica in peanut oil, peanut shell, and chia seeds. J Food Prot 2016; 79(3): 361-8; abstract available at

[Authors: Kuramoto-Crawford SJ, McGee S, Keith Li K, et al]

Communicated by:

[Truffle oil, the implicated vehicle for this outbreak of salmonellosis, is an unusual one. - Mod.LL

A HealthMap/ProMED-mail map can be accessed at:]

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