I am interested in how major foodborne outbreaks and their investigations are interpreted and analyzed: to prevent future outbreaks, minimize the harm from outbreaks that occur, and frame the debates on regulating food safety on farms.
When I was asked by a small organic farmer in California what the implications were of the 2011 O104:H4 European outbreak, I said it could happen here. It also could have worse consequences here.
Let’s review the O104:H4 outbreak conclusions:
In Germany there were nearly 4,000 cases, 54 deaths and 845 cases of hemolytic uremic syndrome (HUS) — unusually, mainly in adults (1) (2).
One hundred percent of the German O104:H4 cases were associated with the production of fenugreek sprouts on a single organic farm in Lower Saxony, with regional distribution centered on Hamburg. The organic farm was found to have satisfactory sanitation and proce- dures and is back in operation.
The epidemiological evidence indicates that a particular lot of fenugreek seed, sold from or produced in Egypt, had become contaminated with this highly unusual outbreak strain. The same outbreak strain was associated with a secondary outbreak in France, also linked to fenugreek sprouts from the same seed lot, but produced as children’s projects and served at a local festival.
Where it starts getting more complicated is that sampling for O104:H4 found no positive results from fenugreek seed lots. There also were no positive results from tens of thousands of environmental samples taken during the post-outbreak investigation, although contaminated sewage and streams were found during the outbreak period. The conclusion was that much better culturing methods were needed for tracking the environmental presence of this pathogen.
Partially confirming data on O104:H4 having a regional origin comes from European tourists, who have become infected with related, but not identical O104:H4 strains after trips to Turkey, Egypt, Tunesia and Afghanistan (3). This supports the idea of regional endemic sources of O104:H4, but not where and how the fenugreek seeds were actually contaminated.
The Egyptian Ministry of Agriculture strongly objected to the identification of Egyptian seeds as the outbreak source in the absence of positive detection of the outbreak strain.
That is where things stand now, with clear identification of the food carrier and the source farm, but with some ambiguity as to the ultimate root cause of the outbreak and the specific mechanism of contamination.
The primary role for epidemiologists and public health officials during a foodborne outbreak, like the O104:H4 outbreak in Germany and France, is to stop the epidemic. If an intervention stops the outbreak, then the identification of the cause is verified. Identification is based on epidemiological evidence; and direct detection is a kind of luxury of evidence. The tools they use have been developed primarily for this purpose, and may be less useful in determining other aspects, such as the search for confirmation of root causes and mechanisms of contamination.
How did the context in Germany shape the investigation and outcome in ways that might be different from the U.S.?
When O104:H4 infections hit Germany, the first “vegetables of interest” were E. coli-contaminated organic cucumbers from Spain, revealed publicly before there was confirmation that the E. coli did not match the outbreak strain. This was curious because of the lack of any outbreak — O104:H4 or other — due to the same two suppliers in Spain itself. Not that any pathogen finding is good, but at least one of the sources was told his cucumbers were seen spilled on the ground at the Hamburg Central Produce market. Perhaps even the non-outbreak pathogens were not due to the farm source. Spanish farmers and the Spanish government saw this as lingering prejudice against Spain.
European Union and German payments were later made to partially compensate Spanish growers.
In contrast, as far as I can tell, there have been no EU lawsuits against the farm for the actual outbreak. So what would be a strict liability case in the U.S. appears to be neither negligence nor foreseeable under the German equivalent law.
There were at least two cultural presumptions, also different in Germany from the U.S. that may reinforce this. Organic appears to be regarded as naturally safer, to the point where the Health Minister was quoted as saying “Of course we know that organic is not really safer.” And fenugreek sprouts were part of a common elaborated sprout cuisine in which sprouts are perceived as a natural healthy food.
U.S. epidemiologists seemed stunned that raw sprouts were not on the top of the list for food surveys in the case/control studies, given the outbreak histories for sprouts. German epidemiologists initially thought including sprouts would only create false positives in case/control studies because sprouts, in general, are so common a food item.
A CDC-FDA-state investigation of a similar outbreak here in the United States would focus more quickly on sprouts given the long history of sprout outbreaks. But perhaps the greatest difference in attitudes is toward organic farming.
Why should Europeans perceive organic farming as safer than conventional agriculture? A substantive reason is that the rules elaborated for organic animal production may provide better protections against transmission of human pathogens, both in the U.S. and the EU. Here I will use U.S. examples.
The Organic Foods Production Act (OFPA), passed in 1990, created the National Organic Program (NOP). Labeling was the basis of the law, that food be correctly identified as organic, but that was the hook for protecting the word “organic” and defining the farming practices.
The U.S. rules for organic compost, in an abundance of caution, were based on EPA guidelines for the use of human waste. This was supposed to provide a wide margin of safety for the use of animal manures. In many studies of E. coli O157:H7 or surrogate pathogen survival under these rules, undertaken since the spinach crisis, it appears that there is a margin of safety even for these STEC but it is not particularly wide.
Organic rules prevented the re-feeding of waste meats from slaughter, including brains and nervous tissue, long before mad cow (BSE) emerged, They ban the non-therapeutic use of antibiotics. They ban the use of dried cow manure as dairy bedding. They require more adequate space for animals and birds so that, for example, de-beaking of chickens is not allowed, or needed due to the insanity produced in birds from overcrowding in a stimulus- deprived environment. The overcrowding of birds, or cattle in CAFOs, may facilitate disease transmission and therefore, in some CAFOs, the routine use of antibiotics, but there also are ranchers who buy antibiotics by the multi-gallon tote without confining their cattle. Most antibiotic sales (by volume) are for animal use in agriculture, between 70 – 80 percent (4).
Organic rules ban the re-use of manures as animal feed.
Last summer, when I was working with a “medium-sized” organic vegetable producer, the price of composted chicken litter (for organic fertilizer) had gone through the roof because of increased demand for pelleted chicken litter in cattle feeding. Thanks in part to the California Leafy Green Marketing Agreement rules, at least there is now research interest in how exactly to p
asteurize different manures for conventional agriculture [for Salmonella, see (5)].
Since it is not an obvious step to feed brains or manure back to cattle, where did this come from? As far as I can tell, many of the changes in conventional animal production after World War II were driven by economists looking for efficiencies in production, without considering biology. They looked at the nitrogen content of manure, for example, and saw inefficiencies in cattle digestion (!) which could be re-captured, rather than fertilizer for soils (6).
All of these factors had to be specifically banned in organic animal production either be- cause they were once routine, or still are routine, in U.S. conventional agriculture. They all could play a role not only in the transmission of human pathogens but in the selection and evolution of more dangerous pathogens: by multiplying and spreading pathogens in closed biological systems, by acting as selection systems for antibiotic resistance and increased tolerance of acidity and other stresses, and by favoring selection for lateral transmission of groups of pathogenicity traits between pathogen species.
Even when there is an underlying substantive basis, EU positive attitudes toward organics may be due more to complex cultural attitudes than to substance.
Food safety criticisms of organic that I hear or read in the U.S. are often based on a failure to understand that most agricultural manures go into conventional agriculture, and for decades only organic agriculture had rules that were specifically designed to prevent human pathogen transmission (7). There is nothing to prevent conventional agriculture from using similar approaches, and sometimes there is a convergence toward safety.
What are some contrasts we could expect in a similar outbreak in the U.S.?
U.S. epidemiologists might identify a sprout-caused outbreak more quickly, and limit the duration of the outbreak.
There would be great differences in the cost of paying for health care, and who is liable for payment.
There would be no compensation to farmers who were misidentified as growing an outbreak crop. There would be no exemption from liability for the farm that caused the outbreak, because they have strict liability for putting out adulterated food.
There would be no presumption that “organic is safer.” There are still major constituencies for whom organic production is an ambiguous, minor but often irritating fact of life in farm and food production industries. They could condemn an outbreak as due to being organic (8), rather than despite being organic, as in the EU.
A final question from the O104:H4 outbreak: what can be done to improve the safety of raw sprouts, whether produced on an organic farm or a conventional farm?
For the actual production process itself there were only two factors: seeds and water. Sprouts were produced with clean equipment in a well-sanitized manner. There is a minimal ecology to sprout production, which may be part of the problem.
Changing from sprouts to greenhouse production of baby vegetables in soil might seem to be a minor change, (let the sprouts grow some true leaves!), but the research on both greenhouse and field production indicates that human pathogen uptake from the soil to plants is highly inhibited, and this can include seed-borne human pathogens.
In a practical sense, sprout safety requires either human pathogen-free seeds specifically produced for sprouting, a kill step that can be used after seeds are sprouted and pathogens are exposed for treatment, or both. People could also cook their sprouts, the original use for soy sprouts from the very beginning of soy as a major food in China (9).
The rational basis for organics includes an ecological approach to farming and an ap- preciation for the biological opportunities and constraints on and around their farms. Conventional farmers can use the same approaches and often do.
I also see sprout production, and the history of sprout outbreaks in this country, as a metaphor for the current approaches to regulating food safety on farm. There could not be a more simplified system for contained and controlled food production than sprouts,
yet it fails repeatedly. Applying the same approaches used in sprout production to the complexity of farms and the farm environment seems both irrational and doomed to fail.
1) Epidemic Profile of Shiga-Toxin-Producing Escherichia coli O104:H4 Outbreak in Germany N Engl J Med 2011; 365:1771-1780 November 10, 2011
(2) STEC Workshop Reporting Group. Experiences from the Shiga toxin-producing Escherichia coli O104:H4 outbreak in Germany and research needs in the field, Berlin, 28-29 November 2011 . Euro Surveill. 2012;17(7):pii=20091. Available online:
Date of submission: 10 February 2012
(3) Eurosurveillance, Volume 17, Issue 4, 26 January 2012 Rapid communications OUTBREAK OF HAEMOLYTIC URAEMIC SYNDROME DUE TO SHIGA TOXIN-PRODUCING ESCHERICHIA COLI O104:H4 AMONG FRENCH TOURISTS RETURNING FROM TURKEY, SEPTEMBER 2011 N Jourdan-da Silva1, M Watrin2, F X Weill3, L A King1, M Gouali3, A Mailles1, D van Cauteren1, M Bataille4, S Guettier4, C Castrale5, P Henry5, P Mariani6, V Vaillant1, H de Valk1
(4) <a href="http://www.wired.com/wiredscience/2010/12/news-update-farm-animals-get-80-of
(5) Appl Environ Microbiol. 2012 Feb;78(4):1302-7. Epub 2011 Dec 16.
Validating Thermal Inactivation of Salmonella spp. in Fresh and Aged Chicken Litter.
Kim J, Diao J, Shepherd MW Jr, Singh R, Heringa SD, Gong C, Jiang X. http://aem.asm.org/content/early/2011/12/12/AEM.06671-11.short?rss=1
(6) The greatest contribution to food safety in the future might be to require biology and microbiology courses for economics students. And there is an interesting possibility that the ethical considerations used in designing organic rules for animals will be shown to also have had long term economic value.
(7) For example, I happened to be at one of the organizing meetings for the CA LGMA when CFSAN investigators revealed that the farm associated with the spinach outbreak was organic in transition. The chief scientist of a major produce organization exclaimed “We were so close!” Perhaps he was under stress. The same attitude came from state senators at a California hearing on the same crisis. “Suppose I don’t want my food grown organic with manures.” Most outbreaks and recalls are in conventional produce and it looks to me like there are fewer outbreaks due to organics than a proportional expectation would predict.
(8) GMO biotechnology companies sometimes have an ambiguous relationship to organic food production. When they want to avoid labeling GMO crops and foods they can point consumers to organics, where GMO is prohibited. When organic farmers block release of crops like GMO herbicide-resistant alfalfa, they get incensed. The USDA’s official position for the last few years has been “people; we can all get along.”
(9) See page 296 of H.T. Huang’s magisterial Fermentations and Food Science; Volume VI: 5 of the series Science and Civilization in China (Joseph Needham). Cambridge University Press, 2000. The first written documentation of soy sprouts in Chinese history includes the steps: wash after three days and fry in oil.