Editor’s Note: With the benefit of a decade of hindsight, The Packer is revisiting the September 2006 E. coli outbreak linked to spinach in a four-part series.
This week National Editor Tom Karst looks at those days when a serious foodborne illness outbreak linked to spinach created a crisis of confidence in produce safety. The coverage this week also reviews the Food and Drug Administration’s investigation and conclusions about its cause. Part two of the coverage looked at how the California leafy greens industry responded to the crisis.  Part three of the coverage looked at how the 2006 spinach E. coli outbreak led to the industry's call for federal oversight.  Part four of the coverage considers what the industry can expect in the next ten years with the implementation and enforcement of the Food Safety Modernization Act.
The crisis of confidence in the status quo of produce safety practices arrived with a thud a little more than 10 years ago. 
Beginning Sept. 14 and continuing until Sept. 20, 2006, the Food and Drug Administration issued daily news releases that flatly advised consumers “not to eat fresh spinach or fresh spinach-containing products until further notice.”
The agency had never before issued such a broad warning about a commodity, said Robert Brackett, who in 2006 was director of FDA’s Center for Food Safety and Applied Nutritions. Brackett is now vice president and director of the Institute for Food Safety and Health at the Illinois Institute of Technology,
“In this particular case all we knew (was) that it was bagged leafy spinach, but we had no idea whose it was or where it was coming from,” he said in December of this year. 
“It was a very scary couple of days because we had all of these serious cases of hemolytic-uremic syndrome popping up and people getting sick, and it was so widespread across the country.” 
The Centers for Disease Control and Prevention reported about half of those who were ill were hospitalized during the 2006 spinach E. coli outbreak.
“It was shocking how little confidence that FDA and consumers had in the produce industry at that moment,” said David Gombas, retired senior vice president of food safety and technology for the Washington, D.C.-based United Fresh Produce Association. 
“For FDA to say ‘Don’t eat any spinach,’ they blamed an entire commodity, and it became very clear to the produce industry at that moment they had to do something to restore public confidence and FDA confidence in the safety of fresh produce,” Gombas said Nov. 30.
“One of the things that was very different and had the greatest impact was the consumer advisory against spinach — period — regardless of where it came from,” said Trevor Suslow, extension research specialist and director of the University of California-Davis Postharvest Technology Center.
The stark warning — immediately followed by steeply falling retail spinach sales — was issued in the midst of a multistate E. coli foodborne illness outbreak eventually linked to Dole brand baby spinach. 
The product was processed, packed and shipped by Natural Selection Foods of San Juan Bautista, Calif., which markets the Earthbound Farm brand. 
U.S. Department of Agriculture data shows that California’s spinach shipments plummeted from 258,774 cartons in August 2006 to 138,278 cartons in September, a drop of nearly 50%. 
Shipping point prices for spinach on the California coast dropped from $8.45-10.45 per carton on Sept. 14 — the day that FDA first issued its advice to avoid for consumers to avoid spinach — to $4.85-6.15 per carton on Sept. 15. 
No market was reported by the USDA for the rest of September because supplies were insufficient to quote.
Counting the cost
The final update on the 2006 spinach outbreak was published by the CDC in October. By March 2007, the FDA issued its own final report about its investigation on the cause of the outbreak.
The CDC said in October 2006 that 199 persons infected with the outbreak strain of E. coli O157:H7 were reported to CDC from 26 states. Later, the tally of those sickened was raised to 205. 
Three deaths in confirmed cases were associated with the outbreak, according to the CDC. The agency said about 80% of the outbreak victims became ill between mid-August and early September.
Gombas said the FDA warning in mid-September caused leafy green sales to crash, not fully recovering for nearly a decade. 
“There were outbreaks before that, but none of them were as devastating to industry or public confidence as that one.”
The FDA and the California Department of Public Health issued a 51-page report on the extensive investigation into the causes of an E. coli O157:H7 outbreak associated with the contaminated Dole brand baby spinach.
The report said investigators identified the environmental risk factors and the areas that were most likely involved in the outbreak. However, they were unable to definitely determine the source of the contamination.
The investigation explored the source of the spinach in 13 bags containing E. coli O157:H7 isolates that had been collected nationwide from sick customers, according to a summary of the report. 
Using the product codes on the bags, and employing DNA fingerprinting on the bacteria from the bags, the investigators were able to match environmental samples of E. coli O157:H7 from one field to the strain that had caused the outbreak, according to the report.
The report said E. coli O157:H7 isolates located on the Paicines Ranch in San Benito had a (pulsed-field gel electrophoresis) pattern indistinguishable from the outbreak strain. The report said the pattern was identified in river water, cattle feces and wild pig feces on the Paicines Ranch, the closest of which was just under one mile from the spinach field.
No smoking gun
According to investigators, the sources of the potential environmental risk factors for E.coli contamination at or near the field included the presence of wild pigs and the proximity of irrigation wells and waterways exposed to feces from cattle and wildlife.
The FDA said that because the contamination occurred before the investigation, the exact means by which the bacteria spread to the spinach remains unknown.
“No definitive determination could be made regarding how E. coli O157:H7 pathogens contaminated spinach in this outbreak,” the report said.
Gombas said there were flaws in the investigation and believes it is impossible to say what batch of spinach was the source of the contamination.
“FDA and particularly the California Department of Public Heath (were) urgently trying to find a source of the contamination so they could make the public feel safe again,” he said. 
“I’ve never been satisfied that the investigation was as good as it needed to be or that it actually found the source of the contamination,” Gombas said.
For example, he said the Paicines Ranch that was ultimately implicated was only responsible for about 500 pounds of spinach, according to what sources at Earthbound Farm told him. 
A spokesman for Earthbound, now owned by Whitewave Foods Co., said the company declined to comment on the story.
What’s more, Gombas said the matching E. coli pattern was found in a creek bed about a mile away from the farm and not on the farm.
Speaking to the difficulty of foodborne illness investigations, Suslow said there will always be challenges in identifying a specific root cause.
“Even with all the most modern techniques in whole genome sequencing, you can’t always identify the specific trigger point,” he said. 
As far as the FDA’s investigation into the 2006 E. coli outbreak linked to spinach, Suslow said the lack of named cause was not necessarily a bad thing.
“We’ve always felt that would have actually been a negative outcome of the investigation, if the conclusion was, ‘We found a case strain indistinguishable in wild pigs, therefore it was a wild pig intrusion,’” he said. 
If that had happened, then any growers who felt they had no pressure from wild pigs may have dismissed the importance of the report.
As it was, the more general concern about wildlife intrusion in fields has been addressed by growers.
While a vector is still hard to identify, Suslow thinks current technology would undoubtedly hasten the investigation and identification of the source compared with 10 years ago, which he said would reduce the scope and impact of a similar outbreak today.
The uncertainty on how the E. coli O157:H7 pathogen contaminated the spinach was not solved, but that did not stop the industry from acting quickly to restore buyer and consumer confidence.
From 1995 to 2006, researchers had linked nine outbreaks of E. coli O157:H7 infections to, or near, the Salinas Valley region. But the 2006 spinach outbreak was different.
There were guidelines for growers in 2006, but not a way to make sure growers were following them, said Joe Pezzini, CEO of Ocean Mist Farms, Castroville, Calif. 
“When the spinach outbreak occurred, it certainly became apparent to me and many others in the industry we needed some sort of mechanism to make sure that people are following good agricultural practices on the farm.”