November 1, 2018
This document provides an overview of factors that potentially contributed to the contamination of romaine lettuce with E. coli O157:H7 that was implicated in a 2018 multi-state foodborne illness outbreak.
- Environmental Assessment Team Approach
- Factors Potentially Contributing to the Introduction and Spread of E. coli O157:H7
- Growing Environment
- Fresh-cut Produce Manufacturing/Processing
- Recommendations for Prevention of E. coli O157:H7 and other Shiga Toxin Producing E. col (STEC) Contamination of Leafy Greens Based on these Findings
- Relevant Links
In early April 2018, the Food and Drug Administration (FDA), in conjunction with the Centers for Disease Control and Prevention (CDC) and state partners, began to investigate a multi-state outbreak of E. coli O157:H7 infections. When this outbreak was declared over by the CDC two months later, it was the largest outbreak of E. coli O157:H7 infections in the United States since 2006, with 210 reported illnesses from 36 states, resulting in 96 hospitalizations, 27 cases of hemolytic uremic syndrome (HUS) and five deaths.
The investigation conducted by FDA, CDC, and state partners determined that consumption of romaine lettuce was the cause of the outbreak. Eighty-seven percent of the cases reported eating romaine lettuce in the week before illness onset. This percentage was significantly higher than results from a survey of healthy people in which 46% reported eating romaine lettuce in the week before they were interviewed. Traceback of the romaine lettuce consumed by ill people determined that it originated in the Yuma produce growing region which consists of farms in Imperial County, California, and Yuma County, Arizona. The traceback identified a total of 36 fields on 23 farms in the Yuma growing region as supplying romaine lettuce that was potentially contaminated and consumed during the outbreak. With the exception of one instance where one of the legs of the traceback led to a single farm, it was not possible to determine which, or how many, of these farms shipped lettuce that was contaminated with the outbreak strain of E. coli O157:H7.
The epidemiological and traceback analyses performed during this outbreak informed an FDA-led Environmental Assessment (EA) of the Yuma produce growing region in collaboration with CDC and state partners from June through August 2018. The EA was conducted to assist FDA in identifying factors that potentially contributed to the introduction and spread of the outbreak strain of E. coli O157:H7 that contaminated the romaine lettuce associated with this outbreak.
The EA team made several visits to the Yuma growing region to conduct its work. During these visits, the team collected numerous environmental samples. Three of these samples were found to contain E. coli O157:H7 with the same rare genetic fingerprint (by whole genome sequencing) as that which made people sick. These three samples were collected in early June from a 3.5 mile stretch of an irrigation canal near Wellton in Yuma County that delivers water to farms in the local area, including several identified in the traceback as having potentially shipped romaine lettuce contaminated with the outbreak strain. This strain of E. coli O157:H7 was not detected in any other samples collected during this EA, although other human pathogens were found in these samples. Because the Yuma region’s growing season had concluded weeks before the EA started, no leafy greens were available for sampling and testing by the EA team.
II. Environmental Assessment (EA) Team Approach
The EA was conducted over several visits by various members of a multi-disciplinary team with expertise in produce safety, agriculture, veterinary medicine, epidemiology, microbiology, environmental health, and sanitation from FDA and the CDC, with valuable contributions from the Arizona Department of Agriculture, Arizona Department of Environmental Quality, and the California Department of Food and Agriculture. Besides the extensive epidemiological and traceback analyses performed during the outbreak investigation, the EA team’s actions and report were informed by inspectional findings of FDA registered food facilities identified in the traceback conducted by FDA field investigators.
The team relied upon the content of the FDA Food Safety Modernization Act (FSMA) Produce Safety Rule and Good Agricultural Practices (GAPs) as the basis for assessing potential contributing factors that could have led to contamination of romaine lettuce on farms identified in the traceback. Areas of focus on these farms included but were not limited to:
- agricultural water,
- soil amendments,
- growing and harvesting practices,
- animal intrusion,
- adjacent land use, and
- employee health and hygiene practices.
Similarly, the EA team and FDA investigators used FSMA Preventive Controls for Human Foods Rule and applicable guidance as the basis for assessing potential contributing factors that may have led to the contamination of romaine lettuce during manufacturing/processing operations in FDA registered food facilities. Areas of focus for the manufacturing/processing operations included but were not limited to:
- facility and equipment sanitary design,
- cleaning and sanitizing practices,
- washing and drying of fresh-cut romaine lettuce, and
- storage of romaine lettuce.
As part of the EA, the team conducted in-depth interviews with produce farm management and fresh-cut produce manufacturing/processing facility management during on-site visits. The traceback investigation identified the locations visited, and the EA team collected information regarding relevant food safety procedures, policies, and practices.
The romaine lettuce that ill individuals consumed was likely harvested between early March and mid-April 2018 based on the fact that reported illness onset dates occurred from March 13 – June 7, 2018. The traceback indicates that the contaminated lettuce had to have been grown on multiple farms and processed at multiple off-farm fresh-cut produce manufacturing/processing facilities. At the time of the EA, no romaine lettuce from the Yuma produce growing region was being grown, harvested, packed or held. However, the EA team still visited farms identified in the traceback as potentially shipping contaminated romaine lettuce that was consumed during the outbreak, where they made observations and, when appropriate, sampled those fields and adjacent areas. FDA also conducted a regulatory inspection and observed manufacturing/processing of leafy greens at a fresh-cut produce manufacturing/processing facility identified via traceback investigation.
The EA team appreciates the cooperation of farms, fresh-cut produce manufacturing/processing facilities, cattle feeding operations, and water districts in the Yuma growing region that were contacted during this investigation.
III. Factors Potentially Contributing to the Introduction and Spread of Pathogenic E. coli O157:H7
Food safety problems related to raw whole and fresh-cut (e.g., bagged salad) leafy greens are a longstanding issue. As far back as 2004, FDA issued letters to the leafy greens industry to express concerns about continuing outbreaks associated with these commodities. FDA and our partners at CDC identified 28 foodborne illness outbreaks of Shiga-toxin producing E. coli (STEC) with a confirmed or suspected link to leafy greens in the United States between 2009 and 2017. This is a time frame that followed industry implementation of measures to address safety concerns after a large 2006 outbreak of E. coli O157:H7 caused by bagged spinach. STEC contamination of leafy greens has been identified by traceback to most likely occur in the farm environment. Contamination occurring in the farm environment may be amplified during fresh-cut produce manufacturing/processing if appropriate preventive controls are not in place. Unlike other foodborne pathogens, STEC, including E. coli O157:H7, is not considered to be an environmental contaminant in fresh-cut produce manufacturing/processing plants.
Well-established reservoirs for E. coli O157:H7 are the intestinal tract of ruminant animals (e.g., cattle, goats, and deer) that are colonized with STEC and shed the organism in manure. Ruminant animals colonized with STEC typically have no symptoms. In contrast, human infection with E. coli O157:H7 usually produces symptomatic illness often marked by severe, often bloody, diarrhea; severe adverse health outcomes or even death can result. Humans shed E. coli O157:H7 in the stool while ill and sometimes for short periods after symptoms have gone away, but humans are not chronic carriers. Various fresh water sources, including municipal well, and recreational water, have been the source of E. coli O157:H7 infections in humans, as has contact with colonized animals at farms or petting zoos. However, most E. coli O157:H7 infections in humans occur from consuming contaminated food.
A. Growing Environment
Known reservoirs of E. coli O157:H7 were assessed in the Yuma growing area, including ruminant animals, water, soil and biological soil amendments of animal origin. There were no E. coli O157:H7 illnesses identified in the Yuma growing region prior to the time of the likely contamination event, therefore a human source for the outbreak is considered unlikely. Sample types collected during the EA included soil, soil drag swabs, wild animal excreta, domesticated animal excreta, biological soil amendments of animal origin, subsurface water, surface water, irrigation canal sediment, and agricultural water. The outbreak strain was identified in three samples of water collected along a 3.5 mile stretch of an irrigation canal in the Wellton area of Yuma, County. No other environmental samples collected in the region yielded the outbreak strain of E. coli O157:H7. It is unknown whether contamination with the outbreak strain in this irrigation canal extended beyond the 3.5-mile stretch.
FDA considers that the most likely way romaine lettuce became contaminated was from the use of water from this irrigation canal, since the outbreak strain of E. coli O157:H7 was found in the irrigation canal and in no other sampled locations. How this process occurred is uncertain, but based on interviews with growers and pesticide applicators, plausible explanations include direct application of irrigation canal water to the lettuce crop or the use of irrigation canal water to dilute crop protection chemicals applied to the lettuce crops through both aerial and land-based spray applications. FDA cannot rule out that there are other sources or means of romaine lettuce contamination that were not identified during the EA investigation.
Information collected by the EA team indicates that, among the Yuma area farms identified in the traceback and that were interviewed, irrigation canal water was only directly applied during germination. However, aerial and ground-based spraying of crop protection pesticides diluted with irrigation canal water occurred at various times during the growing season on a number of these farms, including after a freeze event that occurred in late February. This freeze event likely led to damage of some portion of the romaine lettuce crop, which may have rendered it more susceptible to microbial contamination.
It is uncertain how the outbreak strain of E. coli O157:H7 was introduced into this 3.5-mile stretch of irrigation canal water. The first illnesses in this outbreak occurred in March 2018, and therefore the outbreak strain may have been present in the irrigation canal months before the EA team collected the positive samples, or the outbreak strain may have been repeatedly introduced into the irrigation canal. A large concentrated animal feeding operation (CAFO) is located adjacent to this stretch of the irrigation canal. The EA team did not identify an obvious route for contamination of the irrigation canal from this facility; in addition, the limited number of samples collected at the CAFO also did not yield the outbreak strain. Other possible explanations for how the irrigation canal became contaminated are possible, but the EA team found no evidence in support of alternative explanations.
Growers suggested weather events in the Yuma growing region may have contributed to crop contamination. The EA team considered the possibility that leaf freeze damage and dew on romaine leaves created conditions favorable for windborne contamination of the crop with dust carrying the outbreak strain of E. coli O157:H7. While this type of STEC contamination has been demonstrated (Berry et. al, 2015), it does not explain the presence of the outbreak strain in a free-flowing irrigation canal months later when there was little wind in the region.
B. Fresh-cut Produce Manufacturing/Processing
Low-level E. coli O157:H7 contamination of the romaine lettuce from some of the growing fields identified in the traceback could have been amplified by commingling cut romaine lettuce in wash systems at fresh-cut produce manufacturing/processing facilities. Washing of romaine lettuce either at a fresh-cut produce manufacturing/processing facility or at home by consumers may reduce but will not eliminate pathogens, including STEC, from romaine lettuce. The commingling of romaine lettuce from various farm growing fields at fresh-cut produce manufacturing/processing facilities complicated traceback efforts and made it impossible for FDA to definitively determine which farm or farms identified in the traceback supplied romaine lettuce contaminated with the E. coli O157:H7 outbreak strain. In only one leg of the traceback involving whole head lettuce was FDA able to identify a single farm as having supplied contaminated lettuce. All other traceback legs led to multiple farms as possible suppliers due to commingling during processing. FDA was not able to conduct regulatory inspections and observe the manufacturing/processing of leafy greens at all fresh-cut produce manufacturing/processing facilities identified in the traceback investigation because many of these facilities were not in operation due to the end of the growing season and the manufacturing/processing equipment that may have been used was no longer available for inspection. No deficiencies were found in the single facility which was visited.
FDA has identified the following factors and findings as those that most likely contributed to the contamination of romaine lettuce from the Yuma growing region with E. coli O157:H7 that caused this outbreak.
- The outbreak strain of E. coli O157:H7 was found in water from three locations along a 3.5 mile stretch in an irrigation canal near Wellton in Yuma County, Arizona.
- The outbreak strain was not found anywhere else in sampling done during the EA in the Yuma growing region of Imperial County, California, and Yuma County, Arizona, although other human pathogens were identified in collected samples.
- FDA has concluded that the water from the irrigation canal where the outbreak strain was found most likely led to contamination of the romaine lettuce consumed during this outbreak.
- FDA cannot rule out that other sources or means of romaine lettuce contamination with the outbreak strain of E. coli O157:H7 may have occurred.
- There are several ways that irrigation canal water may have come in contact with the implicated romaine lettuce including direct application to the crop and/or use of irrigation canal water to dilute crop protection chemicals applied to the lettuce crop, either through aerial or ground-based spray applications.
- How and when the irrigation canal became contaminated with the outbreak strain is unknown. A large animal feeding operation is nearby but no obvious route for contamination from this facility to the irrigation canal was identified. Other explanations are possible although the EA team found no evidence to support them.
Fresh-cut Produce Manufacturing/Processing:
- FDA conducted an inspection of a fresh-cut produce manufacturing/processing facility identified in the traceback and found no significant deficiencies.
V. Recommendations for Prevention of Pathogenic E. coli O157:H7 Contamination Based on these Findings
This is the largest STEC outbreak in the United States in over a decade. It has had serious public health consequences as well as ramifications for the produce industry. Leafy greens are a common item in the diet for many Americans and there can be several steps along the supply chain between the farm and the consumer. Measures to prevent contamination are critical along each of these steps. Therefore, all segments of the leafy greens industry should thoroughly review current operations, procedures, policies and practices taking into consideration the findings of this EA, the FSMA Produce Safety Rule, the FSMA Preventive Controls for Human Foods Rule and other relevant FSMA regulations. Other available science-based information relevant to the reduction or elimination of human pathogens on leafy greens should also be considered. Necessary modifications should be made to operations, procedures, policies and practices to ensure safe products for consumers and minimize the likelihood of similar outbreaks in the future.
Outbreaks involving leafy greens can be challenging to investigate because of the short shelf-life of the product, the wide distribution and consumption of leafy greens and the complex supply chain between the farm and the end user. These factors demonstrate the importance of implementation of the FSMA Produce Safety Rule provisions and GAPs on farms as well as the FSMA Preventive Controls for Human Foods Rule provisions, in manufacturing/processing facilities and throughout the supply chain. These provisions are designed to prevent food contamination, foodborne illness, and foodborne outbreaks rather than reacting to them once they’ve occurred.
FDA recommends that growers and processors of leafy greens:
- assure that all agricultural water (water that directly contacts the harvestable portion of the crop) used by growers is safe and adequate for its intended use (including agricultural water used for application of crop protection chemicals);
- assess and mitigate risks related to land uses near or adjacent to growing fields that may contaminate agricultural water or leafy greens crops directly (e.g. nearby cattle operations or dairy farms, manure or composting facility);
- verify that food safety procedures, policies and practices, including supplier controls for fresh-cut processors, are developed and consistently implemented on farms (both domestic and foreign) and in fresh-cut produce manufacturing/processing food facilities to minimize the potential for contamination and/or spread of human pathogens;
- when a foodborne pathogen is identified in the growing or processing environment, in agricultural inputs (e.g., agricultural water), in raw agricultural commodities or in fresh-cut ready-to-eat produce, a root cause analysis should be performed to determine the likely source of the contamination, if prevention measures have failed, and whether additional measures are needed to prevent a reoccurrence; and
- Local in-depth knowledge and actions are critical in helping resolve potential routes of contamination of leafy greens in the Yuma growing region, including Imperial County and Yuma County moving forward. FDA urges other government and non-government entities, produce growers and trade associations in Yuma and Imperial Counties to further explore possible source(s) and route(s) of contamination associated with the outbreak pathogen and with other foodborne pathogens of public health significance. This information is critical to developing and implementing short- and long-term remediation measures to reduce the potential for another outbreak associated with leafy greens or other fresh produce commodities.
Berry, E. D., Wells, J. E., Bono, J. L., Woodbury, B. L., Kalchayanand, N., Norman, K. N., ... & Millner, P. D. (2015). Effect of proximity to a cattle feedlot on Escherichia coli O157: H7 contamination of leafy greens and evaluation of the potential for airborne transmission. Applied and environmental microbiology, 81(3), 1101-1110.
VII. Relevant Links
- Letter to State Agriculture Officials and the Leafy Greens Industry Concerning the Environmental Assessment
- Memorandum to the File on the Environmental Assessment
- FDA Investigating Multistate Outbreak of E.coli O157:H7 Infections Linked To Romaine Lettuce from Yuma Growing Region
- CDC Multistate Outbreak of E.coli O157:H7 Infections Linked to Romaine Lettuce (Final Update)
- About the CORE Network
- FSMA Produce Safety
- FSMA Preventive Controls for Human Foods Rule
- FDA Bad Bug Book