|Outbreak: Jack In The Box Hamburgers|
|Product: Hamburgers||Investigation Start Date: 01/12/1993|
|Location: Multi-State Outbreak||Etiology: E. coli O157|
|Earliest known case onset date: 11/18/1992||Latest case onset date: 02/21/1993|
|Confirmed / Presumptive Case Counts: 503 / 229||Positive Samples (Food / Environmental / Water): 0 / 0 / 0|
|Hospitalizations: 151||Deaths: 3|
This was the largest outbreak of E. coli O157 infections ever documented in the United States, and it injected this pathogen—and threats to food safety in general—into popular consciousness.
- • Associated Bloody Diarrhea and Hemolytic Uremic Syndrome From Hamburgers: The Washington Experience
- • Hamburger-associated E. coli O157:H7 infection in Las Vegas: hidden epidemic
- • A cluster of Escherichia coli O157:H7 infections with the hemolytic-uremic syndrome and death in California
- • Lessons from a large outbreak of Escherichia coli O157:H7 infections
On January 12, 1993, a pediatric gastroenterologist notified the Washington State Department of Health (WSDOH) of an increase in emergency department visits for bloody diarrhea and the hospitalization of three children with hemolytic uremic syndrome.
Hypothesis-generating interviews suggested exposure at Jack In The Box restaurants, and in a swiftly conducted matched case-control study WSDOH confirmed association of illness with Jack-in-the-Box hamburgers.
After news of the Seattle outbreak broke, clusters of bloody diarrhea and lab-confirmed E. coli O157 infections were soon recognized as associated with Jack In The Box hamburgers in California, Nevada and Idaho — an association confirmed by molecular testing by the newly developed Pulsed-Field Gel Electrophoresis (PFGE)method.
Observation of cooking methods revealed that hamburgers did not consistently reach internal temperatures lethal for E. coli. Product trace-backs implicated selected lots of hamburgers (picture); culture of uncooked hamburger patties corroborated the epidemiologic findings. (1)
Several pivotal public-health initiatives were undertaken in this outbreak’s wake:
1. At the time of the outbreak, E. coli O157 infection was reportable in only 12 states. By the end of 1994, 33 states had made it reportable, and by the end of 1996, it was reportable in all but 6 states.
2. The outbreak “broke” the weekend of Bill Clinton’s first Presidential inauguration, and it was one of the first exigencies that faced the new administration. Agriculture Secretary Mike Espy proposed sweeping changes to existing regulations regarding beef production, which had required only visual inspection of beef-processing operations. Under the new rules, USDA began testing samples of raw ground beef in 1994 for E. coli O157, which was declared an “adulterant,” indicating a zero-tolerance policy for its presence even in uncooked beef; and in 1996 required the risk-reduction system known as “Hazard Analysis & Critical Control Points” (HACCP) in meat-processing establishments.
3. A renewed emphasis on foodborne illness was undertaken at CDC. In 1995, “FoodNet” was initiated to capture detailed data regarding foodborne illnesses systematically and to conduct special studies into their sources. Today, food safety has public health prominence as one of CDC’s “Winnable Battles.”
4. The Jack In The Box outbreak was the first major use of PFGE — a new DNA typing technique that could explore relatedness of bacterial isolates. CDC trained and funded state health departments to test bacterial isolates routinely using this method and to report to a centralized system, where widespread but low-level outbreaks could be detected. Today, this “PulseNet” system can be credited with detecting a substantial fraction of recognized foodborne outbreaks.
References: 1. Tuttle et al. “Lessons from a large outbreak of Escherichia coli O157:H7 infections: insights into the infectious dose and method of widespread contamination of hamburger patties.”
|Outbreak: Venison Jerky|
|Product: Venison Jerky||Investigation Start Date: 11/20/1995|
|Location: Benton County, Oregon||Etiology: E. coli (STEC) O157:H7|
|Earliest known case onset date: 11/13/1995||Latest case onset date: 11/20/1995|
|Confirmed / Presumptive Case Counts: 6 / 5||Positive Samples (Food / Environmental / Water): 2 / 2 / 0|
At a time when ground beef was thought to be the source of all foodborne E. coli O157 infections, this was the first documentation of venison-associated E. coli O157:H7 outbreak. Epidemiologists showed that deer can be colonized by E. coli O157:H7 and ultimately be a source of human infections. Game should be handled with the same caution indicated for commercially slaughtered meat, and jerky dehydration does not reliably kill bacteria in meat.
To investigate a 1995 outbreak of Escherichia coli O157:H7 infections in an Oregon community and to assess the safety of meat dehydration methods.
Survey subsequent to routine surveillance report, environmental investigations, and lab experimentation.
Members of an extended household and their social contacts with confirmed or presumptive E. coli O157:H7 infections.
A total of 6 confirmed and 5 presumptive cases were identified. Homemade venison jerky was implicated as the source of transmission. E. coli O157:H7 with the same distinctive, pulsed-field gel electrophoresis pattern seen in the case isolates was recovered from leftover jerky, uncooked meat from the same deer, a saw used to dismember the carcass, and fragments of the deer hide. In a subsequent survey, E. coli O157:H7 was recovered from 3 (9%) of 32 deer fecal pellets collected in nearby forest land. In the laboratory, inoculated venison was dried at several time and temperature combinations, ranging up to 10 hours at 62.8 degrees C. Viable organisms were recovered under all conditions tested.
Deer can be colonized by E. coli O157:H7 and can be a source of human infections. Conditions necessary to ensure the safety of dried meat deserve further review. Game should be handled with the same caution indicated for commercially slaughtered meat.
|Outbreak: Foundation Farm Raw Milk|
|Product: Foundation Farm Raw Milk||Investigation Start Date: 04/10/2012|
|Location: Clackamas, Multnomah and Washington Counties, Oregon||Etiology: E. coli (STEC) O157:H7|
|Earliest known case onset date: 04/01/2012||Latest case onset date: 04/14/2012|
|Confirmed / Presumptive Case Counts: 11 / 5||Positive Samples (Food / Environmental): 2 / 13|
|Hospitalizations: 4||Deaths: 0|
This outbreak highlighted the persistent hazard of raw milk consumption, already well documented in the medical literature. Four of the 11 cases were hospitalized — some critically ill and all with hemolytic-uremic syndrome (HUS), subsequently shown to have been caused by E. coli O157:H7. Although most sales of raw milk are illegal in Oregon, the farm implicated here is an example of one method by which those determined to get the product can skirt the law: instead of “purchasing milk,” families bought “shares” in Foundation Farm cows, their dividends being the milk produced by them and then consumed without pasteurization.
The cause of the outbreak wasn’t long a mystery: Oregon local public health nurses routinely interview each O157 case and ask about “usual suspect” exposures — one of which is whether the case consumed unpasteurized milk. A single case having a high-risk exposure like this one is sufficient to raise suspicion and to warrant further investigation. As the investigation progressed, it transpired that the families that participated in this “cow-share” arrangement had already been aware of many illnesses and communicating among themselves about them; and the dairy farmer had therefore advised the shareholders not to drink the milk. The farm ceased production, and several parents publicly advised the unwary not to serve unpurified milk to their children.
On April 10, 2012, the Multnomah County Health Department was notified by a clinician about a 1 year-old child with HUS (culture pending; later shown to be O157:H7). The child attended a day-care center in Washington County and had a history of regular raw milk consumption, both of which indicated a need for public health follow-up.
Washington County public health officials investigated the child-care facility and identified no other suspected cases there. Meanwhile, Oregon Health Authority (OHA) officials conferred with those from the Oregon Department of Agriculture (ODA) to discuss action that could be taken regarding the herd-share operation that was reportedly the source of the raw milk. It was determined that the operation (dba Foundation Farm), although unlicensed and unknown to Agriculture officials, had been operating legally, with 4 cows, 3 of which were in production. (Dairies of this type are not required to be licensed or regulated in Oregon.) ODA officials contacted the farm owner to request a list of its customers so that they could be contacted and asked about potential illness.
On the morning of April 11th, the farmer reported to ODA that, in the course of contacting his customers through Facebook, he had learned of several additional illnesses. He also reported that he had voluntarily stopped distribution of milk and had recommended to his customers that they discard any available product. Upon request, he sent a list of the 48 household contacts for his customers, and authorized ODA to visit the premises and to collect specimens from the working part of the farm.
That afternoon, while local and state public health officials commenced case finding among herd-share households, OHA investigators and an ODA official visited the dairy farm. They collected 63 samples including rectal swabs on all 4 dairy cows, surfaces in and around the milking parlor, and fecal pat samples from adjacent pastures. No milk was available at the farm for testing.
Over the ensuing days, OHA investigators attempted to interview all households on the list using a standardized questionnaire regarding history of Foundation Farm milk consumption, several other possible food exposures, and diarrheal illness in household members.
(CONTINUED BELOW ↵)
A press release was issued to warn the public about the risk and to stimulate reporting. One of the earliest identified cases was from a household that was not on the customer list: that child had consumed the milk while visiting a family friend.
Leftover raw milk samples were collected for testing on April 12 and 13 from two shareholder households.
Ultimately, 11 lab-confirmed cases—including 1 Washington State resident who consumed the milk while visiting family in Oregon—and 5 presumptive cases were identified. Four other household members reported very mild concurrent diarrheal symptoms and were not counted as cases. Four cases were hospitalized—all with HUS. Three cases were hospitalized for >25 days. Representatives of 30 (62%) of the 48 herd-share households, comprising 91 individuals, were interviewed. All 16 cases had consumed FF milk on one or (usually) multiple occasions. No other suggestive common exposures were identified.
The farm setup was described by ODA as fairly typical for a family farm. The layout was poorly designed from a food-safety perspective. The premises appeared to be difficult to maintain in a hygienic manner for food production. There were no facilities for rapid chilling of milk. Milk bottles were reportedly stored in an ordinary (non-commercial) refrigerator.
Culture of 13 (21%) of 63 samples collected at Foundation Farm yielded E. coli O157:H7; positive samples included 10 of animal manure, 2 cattle rectal swabs and 1 swab of fencing at the milking station. One of two milk samples collected from customer households was also positive. All but one of the O157 strains isolated from cases, milk, and the farm were indistinguishable by 2-enzyme pulsed-field gel electrophoresis (PFGE); 1 case appeared to have an extra band with XbaI digestion.
This outbreak was caused by consumption of unpasteurized contaminated milk. Consumers should be warned that, without a kill step such as pasteurization, there is no reliable way to render milk free of harmful microbes. In particular, E. coli O157 infection can cause bloody diarrhea, hemolytic uremic syndrome and even death.
|Outbreak: Berry Stand Strawberries|
|Product: Strawberries||Investigation Start Date: 08/03/2011|
|Location: Clackamas, Multnomah, Washington, Clatsop, & Yamhill Counties, Oregon||Etiology: E. coli (STEC) O157:H7|
|Earliest known case onset date: 07/01/2011||Latest case onset date: 07/29/2011|
|Confirmed / Presumptive Case Counts: 14 / 1||Positive Samples (Food / Environmental): 4 / 100|
|Hospitalizations: 6||Deaths: 2|
This investigation implicated a novel vehicle—strawberries—as the cause of an outbreak of E. coli O157 infections. An association with locally produced strawberries quickly became apparent as cases were interviewed; but the fact that almost all had purchased them at roadside stands and farmer’s markets led to concern about potential confounding of some overlooked item sold at similar venues. The concern was laid to rest by visits to the stands, a case-control study, and traceback of the strawberries to a single Oregon farmer. Learning how the strawberries became contaminated was the fruit of field work: epidemiologists investigated the strawberry fields and found them heavily contaminated with deer feces, with a herd of deer seen grazing in the area. Culture of 50 environmental samples that contained visible deer pellets yielded E. coli O157 in 10 (20%), with PFGE patterns matching those of the cases.
This outbreak once again confirmed deer as key reservoirs for the pathogen. Interestingly, an additional PFGE-matched case was identified months later; the case hadn’t eaten the commercial strawberries but lived in the area where they were grown. Culture of a sample from this case household’s vacuum cleaning bag yielded a PFGE-matching strain of E. coli O157:H7, a testimony to the pathogen’s ability to survive for prolonged periods when dried.
The following is the abstract from the published article found here. Editorial commentary can be found here.
An outbreak of Escherichia coli O157:H7 was identified in Oregon through an increase in Shiga toxin-producing E. coli cases with an indistinguishable, novel pulsed-field gel electrophoresis (PFGE) subtyping pattern.
We defined confirmed cases as persons from whom E. coli O157:H7 with the outbreak PFGE pattern was cultured during July–August 2011, and presumptive cases as persons having a household relationship with a case testing positive for E. coli O157:H7 and coincident diarrheal illness. We conducted an investigation that included structured hypothesis-generating interviews, a matched case-control study, and environmental and traceback investigations.
We identified 15 cases. Six cases were hospitalized, including 4 with hemolytic uremic syndrome (HUS). Two cases with HUS died. Illness was significantly associated with strawberry consumption from roadside stands or farmers’ markets (matched odds ratio, 19.6; 95% confidence interval, 2.9–∞). A single farm was identified as the source of contaminated strawberries. Ten of 111 (9%) initial environmental samples from farm A were positive for E. coli O157:H7. All samples testing positive for E. coli O157:H7 contained deer feces, and 5 tested farm fields had ≥ 1 sample positive with the outbreak PFGE pattern.
The investigation identified fresh strawberries as a novel vehicle for E. coli O157:H7 infection, implicated deer feces as the source of contamination, and highlights problems concerning produce contamination by wildlife and regulatory exemptions for locally grown produce. A comprehensive hypothesis-generating questionnaire enabled rapid identification of the implicated product. Good agricultural practices are key barriers to wildlife fecal contamination of produce.
|Outbreak: Bagged Spinach|
|Product: Spinach||Investigation Start Date: 09/08/2006|
|Location: Multi-State||Etiology: E. coli (STEC) O157:H7|
|Earliest known case onset date: 08/25/2006||Latest case onset date: 09/13/2006|
|Confirmed / Presumptive Case Counts: 5 / 0||Positive Samples (Food / Environmental / Water): 0 / 0 / 0|
|Hospitalizations: 98||Deaths: 3|
This outbreak highlighted Inter-state health department cooperation. Oregon epidemiologists identified that 4 out of 5 cases in Oregon consumed bagged spinach using their homegrown “Shotgun” hypothesis-generating questionnaire. Contact with WI and NM showed cases already underway with spinach showing signs of being the culprit. Contact with Utah allowed them to quickly re-interview on spinach. The rest played out nationally following a conference call with NM, UT, OR, CDC, and FDA. FDA went public later that day.
- • Final outbreak epidemic curve (MLVA matches only) (PDF)
- • CD Summary Article (PDF)
- • Spinach-focused questionnaire (PDF)
A multi-state outbreak linked to bagged spinach, Dole and others from Natural Selections, Calif.
On Friday, 8 Sept 2006, ~1800, Janie called to report 3 that we had a match of 3 O157s, including 1 from Cowlitz Co. We had 1 form in hand already (GW), so we contacted Debby Uri at home to get the story on her case and attempted to reach Cowlitz Co on-call people. The Linn Co person had been in Idaho the whole exposure period, and presumably was exposed there. GW worked at a hospital in Oregon, but had no contact with any known O157 cases. The Washington guy had been in Oregon only briefly during during the 10 d before onset. His father visiting from Florida had also been ill but no MD. We agreed to pursue jointly on Monday.
Late Tuesday afternoon (again around 1800) Janie reported 2 additional matches, so Melissa took over the task of shotgunning these people. She called until late Tuesday night, and finished Wed morning. The only surprising finding was 4/5 reporting eating bagged spinach, vs. an estimated background for ANY spinach of 17% (P = 0.0036). [Testing months later showed the non-spinach eater to have a different MLVA type.] She had a mix of brands being reported, although 3/5 said they shopped at Winco. Around noon she left to have lunch with a friend and was going to swing by Winco to get sample bags.
Soon after she left I decided to notify CDC that we had a probable hit on this cluster, and to find out if there were any other clusters around the US. Our lab had been unable to upload the patterns because their CDC “fob” had expired, and we were temporarily cut off from the PulseNet data exchange. I sent Chris Braden the picture of the PFGE, and he quickly responded that it appeared by eye to match cases in WI, NM, and UT that were under investigation. He said that WI suspected some kind of fresh produce—possibly based on their demographic profile alone, at which point I emailed that we suspected bagged spinach specifically. (In the earlier message I had said we had a tentative product, but didn’t say what it was. All these exchanges happened within 15-20 minutes). I followed up the 2nd email with a phone call, and he connected us to WI (Jeff Davis and John Archer at least), who had ~17 cases already and were underway with a c-c study.
At that point they had 8 case interviews only, but all 8 had eaten spinach, which for me certainly iced the cake. After that call ended I contacted Utah and NM (not vv as stated in the MMWR). Utah did not have spinach on the Q they were using, but agreed to quickly re-interview on spinach. NM was already interested in spinach from their interviews, and was already trying to collect leftover spinach from 1 hh. During that phone call I got a voice mail from Marilee Poulson that their cases were all reporting bagged spinach consumption.
That is about the end of it. The rest played out nationally following a conference call with NM, UT, OR, CDC, and FDA Thursday morning (14 Sept). FDA went public later that day.
|Outbreak: Cal-Farms Parsley|
|Product: Parsley||Investigation Start Date: 10/20/2005|
|Location: Deschutes County, OR||Etiology: E. coli (STEC) O157:H7|
|Earliest known case onset date: 10/08/2005||Latest case onset date: 10/27/2005|
|Confirmed / Presumptive Case Counts: 3 / 61||Positive Samples (Environmental / Water) 10 / 2|
This 2005 McGrath’s Fish House outbreak of E. coli O157:H7 infections was traced back to parsley from Cal-Farms. The journey to finding the source was interesting: 206 people interviewed, 64 ill people, extremely muddy field conditions, cattle near the flooded parsley fields, and even evidence of heavy deer presence.
On October 20, 2005 we were notified of two E. coli O157:H7 cases from two adjacent counties, Deschutes and Jefferson. Routine follow-up interviews revealed that both ate at a popular restaurant in Bend on the same day, October 12, 2005. Seeing this as a possible common-source exposure, the Deschutes County Health Department in Bend attempted active case finding by obtaining the names of restaurant patrons who used credit cards on October 12th. An initial quick survey identified several other diners who reported gastrointestinal symptoms after their meal. A formal case-control study was launched using an expanded list of credit card names from October 12-15, and a questionnaire based on restaurant menu as well as characterization of illness, if any.
Names from the credit card list were used to look up telephone numbers on the Internet. Deschutes County staff and MPH students from the Acute and Communicable Disease Program (ACDP) of the Oregon Department of Health Services interviewed people. Several people reported gastrointestinal illness after eating at the restaurant. On October 23, 2005, the Deschutes County Health Department decided to issue a press release. Medical alerts were sent to the local physicians and emergency rooms. The press release stimulated additional reports of illness. E. coli O157:H7 isolates were subtyped by pulse-field gel electrophoresis (PFGE) People who reported GI illness were asked to submit stool specimen for confirmation. Some gave specimens to the local health department, while others gave specimens to their doctors.
The Deschutes County Environmental Health section inspected the restaurant. Employees were asked about recent GI illness. Environmental samples and food samples were collected.
We visited Cal-Farms in Oregon City, reviewed their operations, and obtained parsley sales records for September and October. We were shown 2 fields that were the source of parsley harvested in September and October, and collected ~100 convenience samples of soil and parsley stubble on November 7th from both fields. There were no obvious deficiencies in operating conditions to these inexpert observers. Several potential sources of O157 were noted, including livestock in nearby fields (goats, lamas), river water used for irrigation (in drier months), and a deer presence heavy enough to merit repellent next to parsley fields. Because extremely muddy conditions made it difficult to seal sample bags, these were pooled into 6 composite samples – 3 from each field. These samples were enriched and tested by multiplex PCR and cultured on CT-SMAC for O157 at the Institute for Environmental Health (Lake Forest Park, WA; courtesy Dr. Masour Samadpour).
A total of 206 people were interviewed, including people who called in after the press release was issued. Of 120 completed interviews derived from the credit card names, 33 (27%) reported GI illness, of whom 23 (19%) met a working case definition (three or more loose stools in a 24 hour period, and incubation period > 1 day and < 10 days). In total, we identified 64 people who reported three or more loose stools (Figure 1). The median incubation period was 2.6 days. Forty-three (67%) were females, and the median age was 51 (range 4-87). Meal dates for those who were ill were from October 2 – October 22 (Figure 2).
Symptom profile is shown on Table 1. Twenty-one people reported having bloody diarrhea, and only 7 (33%) of these sought medical care. Of those who sought medical care, 6 (86%) were asked to give stool specimen.
By our initial univariate analysis, crab and artichoke dip, coconut prawns, and vegetables were all significantly associated with illness, but none of these items accounted for more than 20% of the cases.
As we were considering these results, first-enzyme PFGE results on the initial isolate were posted to PulsNet revealing a match to a recently investigated cluster (2 restaurant groups, and 2 sporadic cases) in Washington. Washington epidemiologists had identified parsley (traced to an Oregon supplier and grower) as the likely vehicle for those cases. Armed with this knowledge, we then considered parsley as a potential vehicle for the McGrath’s outbreak. We determined that parsley from the same supplier (Pacific Coast Fruit) and farm (Cal-Farms, Oregon City) had been the sole source of parsley at McGrath’s from XX through ~ October 10 (last delivery date on October 10th). Parsley was used on a large number of menu items, including several side dishes that unfortunately had been omitted from the questionnaire. We reanalyzed our data, using a composite variable standing in for all the food items served with parsley. Limiting the analysis to meal dates from October 12-15 and adding abdominal cramps to the case definition, we found parsley to be significantly associated with illness (OR=3.32, p-value = 0.02). This variable could explain about 80% of the cases. Other food items that were significant included vegetables (OR=3.18, p-value = 0.02) and red potatoes (OR=4.44, p-value = 0.03), both of which had parsley. Interestingly, we learned that the crab and artichoke dip was always served with parsley-topped bruchetta.
Food samples and environmental samples tested negative at the Oregon State Public Health Laboratory (OSPHL). Water and the filter from the ice machine were tested, and were negative.
|OR = 3.32||95% CI = 1.11-10.39||P-value = 0.028|
|OR = 3.18||95% CI = 1.11-9.18||P-value = 0.027|
|OR = 4.44||95% CI = 0.98-21.10||P-value = 0.03|
Parsley from Cal-Farms was the apparent cause of the McGrath’s outbreak, by extension, all recent Oregon and Washington cases with matching PFGE. The only food item that explained most of the cases was the parsley. The fact that the three confirmed cases matched the Washington cluster suggest a common source. Seven of the 8 cases in Washington had foods that had parsley, and the parsley came from the same grower. The Washington cases had other things in common, such as romaine lettuce, roma tomatoes, red cabbage, and onions, but these food items came from different distributors.
The parsley farm distribute to various places including grocery stores. Pacific Coast Fruit, the distributor for the restaurant, is only one of a number of their customers. It is not clear why this distributor would get a contaminated batch and why only a few restaurants would get contaminated parsley. This wholesaler got about 28% of the sales from 9/1/05 – 10/28/05.
We would have expected to see a lot more cases since the parsley was distributed to other places too.
During the visit to the farm, a number of possible sources of contamination were noted. There were deer repellents, and deer tracts. Samples of parsley and dirt were tested, but were negative.
Only 3 cases were confirmed out of 64 ill people. Five additional cases were tested, but no E. coli O157 were detected. The specimens were collected 9-15 days after onset of diarrhea. Most adults do not excrete the organism after ~2 weeks, and 3 weeks in kids. Three cases were tested through their private physicians, and
were negative. Interestingly, most cases did not seek medical care, even those with bloody diarrhea. Of those with bloody diarrhea, 33% sought care, and of these, 86% were cultured.
The restaurant voluntarily closed on October 24th and was cleaned thoroughly. All the food workers were tested and were negative. The restaurant was reopened on November 1st. We did not hear of new cases after the restaurant was reopened.
The recommendations were:
1) Throw out all left over foods.
2) Emphasize employee hand washing.
3) Ill employees should not work until symptoms resolve, or if they are culture positive for E. coli O157, they should have 2 negative stools before returning to work.