Tag Archives: oregon health authority

Hydro-Harvest alfalfa sprouts

Outbreak: Hydro-Harvest alfalfa sprouts 
Product: Alfalfa sproutsInvestigation Start Date: 02/01/1999
Location: Multi-State: OR, WA, ID.Etiology: Salmonella Mbandaka
Earliest known case onset date: 01/09/1999Latest case onset date: 06/12/1999
Confirmed / Presumptive Case Counts: 43 / 0Positive Samples (Food / Environmental / Water) 12 / 0 / 0

The increasing popularity of sprouts as health foods was sharply followed by the epidemiologic discovery that sprouts are prone to transmitting foodborne pathogens like Salmonella. This was the largest “sproutbreak” of foodborne salmonellosis in Oregon since the multistate and multinational outbreak of Salmonella Newport infection in 1996, in which alfalfa sprouts were also implicated as the vehicle of transmission.


Since 1995, sprout products (alfalfa, clover, radish, mung bean) have become recognized as common vehicles for enteric pathogens including Salmonella, Escherichia coli O157, and Listeria. Outbreaks have been recognized repeatedly in Europe (notably Scandinavia), North America, and Japan. Most of these outbreaks have been traced to the use of contaminated seed, in which pathogens proliferate during germination. Seed lots are often quite large (≥18,000 kg) and may be distributed to numerous growers in widely dispersed locations. Outbreaks often manifest as cases scattered across several states or countries, and can persist for months, reflecting the stability of the pathogen on dried seeds.

The only completely reliable way to prevent sprout-associated illness is abstinence. In the United States, several state health departments, the FDA, and other agencies have issued statements discouraging raw sprout consumption. Because of the increased risk for severe infection with at least some sprout-associated pathogens (notably Salmonella and Listeria), these warnings are often targeted at immunocompromised individuals. Most persons who become ill in outbreaks are immunocompetent, however.

Many people enjoy eating sprouts, and many people make a living growing, processing, and distributing these products. In consequence, food scientists and members of the sprout industry have investigated procedures to improve the safety of sprouts. These efforts have concentrated on chemical disinfection of seeds immediately prior to germination.

Laboratory studies suggest that treatments with sodium hypochlorite or calcium hypochlorite can reduce Salmonella loads on artificially inoculated seeds to undetectable levels. Calcium hypochlorite (at 20,000 ppm) has been strongly recommended, because higher disinfectant levels are achievable without unacceptable reductions in germination rates.

Some outbreaks provide natural experiments that shed light on the effectiveness of seed disinfection. Oregon Public Health Division epidemiologists investigated one such outbreak in early 1999.

By law, all Salmonella isolates identified by Oregon laboratories are forwarded to the Public Health Laboratory for serotyping. Similar law or custom obtain in Washington, California, and Idaho. Salmonella Mbandaka is uncommon in Oregon (1988–98 mean, 1.5 cases/year). When 3 Mbandaka isolates were identified within a week in January 1999, it was not difficult to surmise that a common-source outbreak was occurring. Surrounding states and CDC were notified immediately. Initially, reported cases were confined to Oregon.    (CONTINUED BELOW ↵)

Preliminary interviews were conducted with cases or household informants by local health department nurses using standardized case investigation forms. Sprouts—a perennial suspect in geographically dispersed outbreaks of salmonellosis—quickly became a focus of the investigation.

Investigators compared exposure histories of the first 10 Oregon cases reported with those of age- and phone prefix-matched controls. We traced sprouts consumed by cases to their origins.

Information about later cases was collected by public health agencies in Washington, Idaho, California, and Oregon. Environmental investigations at produce retailers and wholesalers and with sprout growers and seed distributors were conducted by the Oregon and Washington Departments of Agriculture, the California Department of Health and Human Services, and the FDA. Sprouts and seed samples were collected and cultured for Salmonella.

Initial suspicions that commercially distributed alfalfa sprouts were the source (based on demographics, case distribution, and preliminary food histories) were corroborated by case-control study results. Nine of the first 10 cases recalled alfalfa sprout consumption vs. 0/20 controls (p=0.002). Among cases who had consumed sprouts, 8/9 reported definite (N=5) or possible (N=3) consumption of Hydro-Harvest sprouts (see Product Traceback figure). No other plausible source was identified.

On February 12, press releases were issued announcing a voluntary recall of all Hydro-Harvest sprouts. S. Mbandaka was later cultured from alfalfa sprouts and ungerminated seed collected at the Hydro-Harvest facility. Outbreak-associated cases were eventually identified in four states (see Epidemic Curve): Oregon (N= 40), California (N= 21), Washington (N= 19), and Idaho (N= 5).

A common outbreak pattern was identified by molecular typing (PFGE and micro-restriction fingerprinting). This pattern differed from those of “sporadic” isolates obtained before the outbreak, which were heterogeneous.

The implicated seed came from an 18,000-kg lot milled from alfalfa grown in Southern California. By the embargo date, seed from that lot had been distributed to 4 growers in California, 1 in Florida and Hydro-Harvest in Washington (see Seed Distribution figure); one grower had not started to use it. Cases were eventually linked to only 2 of the 5 growers that had sold sprouts from this lot, however: Hydro-Harvest (OR, WA, ID cases) and brand Y in San Diego (CA). Although documentation was incomplete, the 3 sprouters    (CONTINUED BELOW ↵)

that were not linked to any cases (and who used 41% of the seed) allegedly disinfected with 20,000 ppm calcium hypochlorite or 500 ppm sodium hypochlorite.

This outbreak provided an imperfect natural experiment to assess the efficacy of alfalfa seed disinfection. The observation that—cases were attributable only to the growers who did not disinfect seed–is consistent with, though not proof of, the hypothesis that seed disinfection can reduce the risk of salmonellosis for sprout consumers.

Seed disinfection procedures could not be verified at any site. No sites, including those who allegedly used the FDA-recommended 20,000 ppm calcium hypochlorite soak, maintained any sort of production log or similar, contemporaneous documentation of disinfection practices. The germination procedures, undertaken by Hydro-Harvest and grower Y, could not be independently verified.

Whether contamination within seed lot 8119 was uniform could not be assessed, but, S. Mbandaka was recovered from almost every sample tested (both from ready-to-eat sprouts and from seed collected Hydro-Harvest, grower Y, and the originating warehouse).

The number of reported cases reflects to some extent publicity about the outbreaks, which differed from state to state. Most importantly, data from other outbreak investigations indicate that even the preferred 20,000 ppm calcium hypochlorite disinfection can be inadequate under at least some circumstances. Seed disinfection may be better than nothing, but it is unclear how much.

Sprout growers should routinely document seed disinfection methods, and outbreak investigators should carefully review and report these practices. As these data accumulate, we will get a better sense of how effective seed disinfection is.

Sprouts continue to pose a risk for all consumers. Despite episodic publicity, many consumers remain unaware of this risk. Public health advisors should consider ways to increase awareness of this hazard, particularly among high-risk individuals.

Cal-Farms Parsley

Outbreak: Cal-Farms Parsley 
Product: ParsleyInvestigation Start Date: 10/20/2005
Location: Deschutes County, OREtiology: E. coli (STEC) O157:H7
Earliest known case onset date: 10/08/2005Latest case onset date: 10/27/2005
Confirmed / Presumptive Case Counts: 3 / 61Positive 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.

Environmental Inspection
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.

Bloody diarrhea1727%

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 = 3.3295% CI = 1.11-10.39P-value = 0.028
OR = 3.1895% CI = 1.11-9.18P-value = 0.027

Red PotatoesCaseControlTotal
OR = 4.4495% CI = 0.98-21.10P-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.