Pending External Review Key Facts
- Romaine lettuce accounts for 30% of the lettuce consumed in the United States. Between 1990 and 2009, per capita consumption increased from 1.2 to 7.7 pounds per person.
- Although contamination of marketplace product is rare, between 1998 and 2018, at least 34 romaine lettuce-associated outbreaks were reported to CDC’s National Outbreak Reporting System (NORS), causing 1,040 illnesses, 256 hospitalizations, and 5 deaths.
- The majority of romaine produced and consumed in the U.S. currently comes from California and Arizona. The bulk of romaine lettuce is hand harvested, although mechanical harvesters are used by some operations.
- Small numbers of bacterial pathogens may survive on field lettuce for one or more weeks after contamination.
- Between 2000 and 2020, at least 42 romaine lettuce-associated outbreaks were reported to CDC’s National Outbreak Reporting System (NORS), causing 1,314 illnesses, 365 hospitalizations, and 5 deaths.
- One of the most recent recalls occurred in 2021 due to possible Listeria monocytogenes which has since then, ended.
- Chlorine or other sanitizers are used in wash water to prevent cross-contamination of lettuce.
- For video instruction on how to wash a head of romaine lettuce, please visit Food Smart Colorado.
Pending External Review Content
Lettuce (Lactuca sativa L.) is a popular vegetable that is widely grown and consumed throughout the world. China is the largest producer of lettuce, contributing 55% to the world’s total production by weight. By contrast, the United States contributes only about 16% to total lettuce production worldwide. The primary type of lettuce produced and consumed in China is a stem lettuce (L. sativa L. var. angustana), while in the U.S. there are three main lettuce types produced: iceberg (L. sativa L. var. capitata), romaine (L. sativa L. var. longifolia), and leaf (L. sativa L. var. crispaa). These three lettuces account for 54.1%, 30.1%, and 15.8% of U.S. production, respectively.
Lettuce comes in a variety of colors, sizes, and shapes. Romaine lettuce is exceptionally crisp, slightly bitter, and is characterized by long, narrow leaves with thick ribs. The leaves are typically upright and form an elongated head (the top of the head may or may not close over the inner leaves), with commercial heads typically weighing approximately 0.75 kg. Romaine lettuce is well known as the primary ingredient in Caesar salad, but in foodservice arenas it is now included in a variety of sandwich wraps, entrées and Greek salads. It is also included in the supermarket sections as prepackaged romaine hearts and in a wide variety of prepackaged salads. Although not as popular as iceberg lettuce, from 1990 to 2009, the per capita consumption of romaine lettuce increased from 1.2 to 7.7 pounds per person.
Romaine lettuce is typically grown under conditions where contamination with enteric pathogens (Salmonella, Escherichia coli O157:H7, Listeria monocytogenes, Cyclospora cayetanensis, etc.) is possible; therefore, depending on the level of contamination and the health of the individual, consumption of the raw product could lead to illness.
Foodborne Outbreaks and Recalls
Foodborne outbreaks from contaminated, fresh leafy vegetables are increasingly being seen in many parts of the world. In the U.S., there have been several high-profile outbreaks specifically associated with the consumption of romaine lettuce (see table below). Between 2000 and 2020, at least 42 romaine lettuce-associated outbreaks were reported to CDC’s National Outbreak Reporting System (NORS), causing 1,314 illnesses, 365 hospitalizations, and 5 deaths.
Since these outbreaks in the early 2010s, additional multi-state outbreaks have occurred in the United States. In 2018, two outbreaks of E.coli led to over 100 hospitalizations and 5 deaths, the first of which occurred in April 2018. A total of 210 people across 36 states were infected with an outbreak strain of E. coli O157:H7 leading to 27 cases of hemolytic uremic syndrome (kidney failure) and 5 subsequent deaths. Investigation linked the outbreak to romaine lettuce grown in the Yuma region. Environmental samples taken in the Yuma growing region found the E. coli outbreak strain in water from an irrigation canal. During the investigation, romaine lettuce production and distribution was paused in the Yuma region to reduce potential exposure to the contaminated product.
Months later in October 2018, a separate multi-state outbreak of E. coli O157:H7 occurred across 16 states. Of the 62 people infected, 25 were hospitalized with two reported incidences of hemolytic uremic syndrome and no reported deaths. Whole genome sequencing of the outbreak strain found that the DNA fingerprint was unrelated to the E. coli O157:H7 outbreak earlier in the year. Traceback investigation identified romaine lettuce as the outbreak source, linking back to the Central Coast growth region of northern and central California. The outbreak strain was identified through environmental sampling in both water and sentiment samples at Adam Bros Farming in the region.
From September to December 2019, a multistate outbreak of Shiga toxin-producing E. coli (STEC) was reported across 27 states. A total of 167 individuals were infected, with over half of infections resulting in hospitalizations (85 people) and 15 people developing hemolytic uremic syndrome. Investigation into the outbreak identified romaine lettuce grown in the Salinas Valley of California as the contamination source. The outbreak strain of STEC was detected in fecal-soil composite samples taken from cattle grazing lands adjacent to farms used to grow romaine implicated in the outbreak.
A 2020 multistate outbreak of E. coli O157:H7 infections was linked to leafy greens, including romaine lettuce. A total of 40 individuals were infected across 19 states, leading to 10 reported hospitalizations and 4 cases of hemolytic uremic syndrome. Epidemiologic investigation identified leafy greens as the probable source of the outbreak, however no specific type or brand of leafy greens were able to be identified. Of 23 ill people interviewed, 22 reported eating leafy greens wherein 15 consumed romaine. Identifying a specific type was made difficult due to overlaps in growing, harvesting, and processing seen with leafy greens; while several farms of interest were identified, no single source was found.
A recent recall was conducted in December of 2021 due to possible contamination of Listeria monocytogenes. Fresh Express packaged and bagged salads including 50/50 mixes, spinach, romaine, and iceberg were recalled in more than 15 states with at least 10 illnesses. The recall has since then ended.
Although outbreaks are cause for concern, based on pathogen prevalence surveys conducted on romaine lettuce in the marketplace (see table below), the industry has appropriate safeguards in place which minimize the risk for consumers to encounter a contaminated product.
It is noteworthy that the majority of survey data only reports whether enteric pathogens such as Salmonella and E. coli O157:H7 were present or absent. There is rarely an indication of the number present nor the virulence of the isolate, which together would affect the risk of infection if that item was consumed raw. Variations in the methods used for detection of the pathogens in lettuce also exist with different surveys. This data may only be signifying that a viable pathogen has been present but not whether it is still viable and able to cause illness.
In the U.S. over a 20-year span (1992–2012), yields of romaine lettuce increased from 31.7 to 35.6 t/ha for an average increase of 12%. While shifts in market use, such as a reduction in the proportion of the head harvested for romaine lettuce hearts, negated some of the increased yields, changes in agronomic practices (e.g., wide beds and high plant density) and the use of more uniform and disease and pest-resistant cultivars are largely responsible for the increased yield gains.
Romaine lettuce is classified as a cool-season crop and is grown in moderate climates with optimal day-time temperatures of 7 to 24°C and night-time temperatures of 3 to 12°C. At the high end of the temperature range, lettuce becomes more bitter, has a tendency to bolt (premature flower stalk formation), and generates loose, fluffy heads. At temperatures near freezing, growth is slowed without damaging young plants; however, the outer leaves of mature lettuce plants may be damaged at low temperatures.
In the United States, the bulk of lettuce production occurs in two states, California and Arizona. Together, they provide a year-round supply of lettuce for domestic consumption. Other states that devote commercial acreage to seasonal lettuce production include Colorado (July to September), Florida (December to April), New Mexico (April to May), and Washington (June to September). In these areas, soils used for cultivation should be well-drained and rich in organic matter. The majority of soils meeting those criteria within California are classified as silt loams or sandy soils. Heavy clay soils may also be used to grow lettuce if they have good soil structure for adequate drainage.
Within the major growing areas of the U.S., romaine lettuce is typically cultivated on raised beds (4 to 10 in) that may be either narrow (40 to 42 in) or wide (80 to 84 in). On these beds, pelleted seed is deposited just below the surface in two or three (narrow beds) or five or six (wide beds) parallel rows, using a precision planter. Transplants are typically seeded into cell plug trays in the greenhouse four to six weeks prior to going to the field. In major production areas, transplanting may be selected at the start of the season, or at midseason, when there is a need to get a crop in to meet production schedules. Transplanting is also used extensively in organic production. In minor production areas, transplants may be preferred due to the short growing season.
Several types of irrigation (sprinkler, drip, and furrow) are used to provide continuous moisture, which allows for maximum yields and quality. Initially, sprinkler irrigation (2 to 4 in) is used prior to seeding to soften the soil for seedbed preparation. Then every two to three days, water is applied to seeded soil or transplants until seeds emerge or transplants have been established (usually 6 to 10 days after transplanting). Irrigation continues for the remainder of the growth cycle, with the highest use of water occurring during the last month of crop growth. During this time, surface drip irrigation with drip tape is often installed and utilized as it permits growers to water frequently during this rapid vegetative growth phase. This type of irrigation is also advantageous because romaine lettuce is shallow-rooted, and drip irrigation, rather than sprinkler overhead irrigation, is more effective at delivering water directly to the roots. Therefore, less water is required (12 to 18 in for drip compared to 18 to 24 in for spray irrigation). Drip irrigation also facilitates weekly fertigation with low rates of fertilizer as opposed to having to apply side-dressings of nitrogen close to the romaine lettuce roots (applied typically two to three weeks after seeding and thinning has taken place). When used, drip tape is installed between rows and typically retrieved before harvesting so that it may be reused for subsequent crops. Furrow irrigation, the least efficient in terms of water usage (24 to 30 in), is used primarily in Arizona, which has an abundant water source from the Colorado River and is a much cheaper option for producers there.
Several other growing practices may be used to extend the growing season of romaine lettuce, including growing plants in high tunnels, greenhouses, or in hydroponic systems. In Florida, the use of hydroponic systems has grown rapidly. The predominant hydroponic design uses plastic or other lightweight channels, gutters, or tubes that hold multiple transplants. A thin film of nutrient solution trickles over the bare roots of each plant. The whole system is at a sloped angle, enabling catchment of the unused nutrient solution, which is then filtered or aerated and recycled back to a reservoir for reuse. However, Hydroponics remains a very expensive option and makes up a very small portion of commercial growers.
Harvesting and Postharvest
Historically, romaine lettuce has been hand harvested as whole plants; however, small growers selling bagged greens may choose to harvest the crop as individual leaves. Typically, the time for romaine lettuce to reach market maturity will depend on growing conditions and variety. Waiting too long to harvest can result in bolting. Once the romaine head is cut at the base, the head is trimmed of loose, discolored, damaged, diseased, and soiled leaves. The heads are then placed on a conveyor belt where they are sprayed with a chlorinated water solution (generally 200 ppm) before being packed into 24 count (head) cartons.
Hand harvesting of lettuce requires a large amount of human capital. For example, in Arizona, more than 45,000 legal guest workers from Mexico are commuted across the border into Yuma every day for the purposes of harvesting up to 1 million boxes of lettuce each day. Automated, mechanized romaine harvesters, which use a water knife to cleanly cut the heads in the field, are now being used in some commercial operations.
Romaine lettuce heads have moderate respiration rates, which are generally higher than rates for iceberg lettuce. Therefore, it is even more critical that the product is quickly cooled to extend its shelf-life. Cartons of romaine lettuce are shipped to a facility where field heat is generally removed through vacuum cooling. Once these operations are performed, romaine typically has a storage life of two to three weeks if stored at the proper temperature (0 to 5°C) and relative humidity (95%). Although low oxygen atmospheres will reduce respiration, atmospheres containing carbon dioxide are not generally beneficial to intact heads. In contrast, cut romaine lettuce is commonly packaged in low oxygen (<1%) and high carbon dioxide (7 to 10%) atmospheres because these conditions control browning on cut surfaces.
The majority of romaine lettuce worldwide is grown in open agricultural systems. In such systems, pathogen contamination may arise from several contaminated sources, including animal manure-based soil amendments, irrigation water, run-off water from livestock operations, insects, aerosols, and wildlife fecal matter. The extent of crop contamination varies with the contamination source but may be anything from a localized event to the entire crop being contaminated. In addition, even if the pathogen does not get deposited onto the plant’s surface, there is the potential for it to be later contaminated through indirect events such as water splashing contaminated soil or wildlife scat onto the plant.
When a pathogen comes into contact with the phyllosphere (aerial) tissue, distribution on the surface is highly variable and likely a reflection of variations in the chemical compounds and physical topography at individual sites. Some studies have shown that Salmonella tends to localize preferentially near the leaf stem and leaf underside rather than the leaf blade and topside. Internalization of both Salmonella and E. coli O157:H7 into the phyllosphere tissue has also occurred with the pathogen entering via the stomata. Similarly, a large portion of E. coli O157:H7 that is deposited on a plant’s surface is quickly inactivated; however, there is a slower rate of decline of the surviving cells. For example, when E. coli O157:H7 was deposited on the upper surface of romaine lettuce heads in the field, within two hours after being exposed, the pathogen population had already been reduced a thousand-fold. Four weeks after exposure, however, a low number of surviving cells could still be detected.
Two main environmental factors are primarily responsible for the initially rapid pathogen inactivation that occurs on lettuce plants: ultraviolet radiation and desiccation. It has been theorized that surviving pathogen cells are those that have been deposited into niches where exposure to these two environmental factors are minimized. Because niches provide protection from ultraviolet radiation and desiccation, the pathogens may have sufficient time for the cells to modify their metabolism and become more stress-resistant.
Enteric pathogens on romaine lettuce are also affected by other biological agents. For example, E. coli O157:H7 is more persistent on romaine lettuce when the plant pathogen responsible for downy mildew disease is also present. For example, the levels of culturable indigenous bacteria showed significant positive correlations to the titers of multiple surrogate enteric viruses on romaine lettuce, whereas there was no effect on the survival of E. coli O157:H7 when field-grown microflora was transferred onto romaine lettuce plants being cultivated in a growth chamber. In contrast, indigenous microflora present in the rhizosphere (soil located in close proximity to the roots) is conjectured to impede the internalization of enteric pathogens through the roots of lettuce plants. This conclusion was based on the observation that in field soils having large numbers of indigenous microflora, internalization into roots only occurred when enteric pathogen populations were artificially added to the soil to levels that would not occur naturally (i.e., more than a million cells per gram). In contrast, there have been two scenarios where internalization of enteric pathogens into roots has been observed at lower pathogen levels. In one case, the plants had been growing in field soil that had been subjected to high heat to dramatically reduce the native microflora. In the other case, the plants were being cultivated hydroponically and thus there would be much lower levels of microflora present in the water than would be present in soil.
Contamination of romaine lettuce may occur anywhere along the farm-to-fork continuum. Therefore, management and regulatory guidelines (to avoid contamination) and interventions (to reduce cross-contamination and/or contamination) have been developed for application throughout the continuum.
Post-harvest leafy greens (both prepackaged and head lettuce) are typically washed thoroughly or submerged in water for five to 15 minutes to remove soil and debris before being refrigerated. This gives products a fresh look and crispy texture. However, submersing leafy greens in water can potentially dislodge enteric pathogens from contaminated products and release them into the water. Those pathogens may then be transferred to uncontaminated lettuce and processing equipment surfaces. Including sanitizers such as chlorine (sodium hypochlorite) or peroxyaectic acid (Tsunami) during washing operations has been shown to be effective at mitigating cross-contamination. Due to its wide antimicrobial activity and low cost, chlorine is the most common sanitizer used for washing lettuce. Concentrations of 50 to 200 ppm and contact times of one to three minutes are recommended. However, one disadvantage to using chlorine is its high reactivity with organic matter which decreases the levels of active chlorine in the water that is capable of inactivating pathogens. Although inclusion of a chlorine-stabilizer, T-128, has been shown to extend the efficacy of chlorine when high organic loads are present in the wash water, there is also public concern that trihalomethane by-products formed in the presence of organic matter during disinfection of drinking water would also be formed in wash water. Chlorine dioxide has been suggested as an alternative to sodium hypochlorite for a wash water sanitizer as the former possesses higher oxidation capacity and forms fewer halogenated by-products than the latter.
A wide assortment of antimicrobials, including organic acids, ozone, and the sanitizers discussed above, have been examined for their efficacy in reducing field-acquired contamination on lettuce. For the majority of these antimicrobials, the efficacy has been relatively low, resulting in only a 10 to 1000-fold reduction of the pathogen per gram of romaine lettuce. Varying success for pathogen inactivation has also been achieved with different physical (ultraviolet light, ultrasound, irradiation, cold atmospheric plasma) and biological (antagonistic bacteria, bacteriophages, bacteriocins) interventions. Although the majority of those studies have not sought to differentiate the response of pathogens residing at different locations, internalized pathogens would likely be unaffected by aqueous antimicrobial treatments compared to physical interventions. However, with any intervention that shows promise for inactivating pathogens on romaine lettuce, it is critical that, prior to commercial implementation, verification be made as to whether the intervention treatment affects the product’s quality either initially or during storage. At present, these pathogen-reducing interventions are not being adopted by the industry because there is concern that any increased cost associated with the treatment would likely be transferred to the consumer who would find it unacceptable.
As noted earlier, romaine lettuce, whether as heads or in a packaged salad mix, should ideally be held at refrigeration times (0 to 5°C) during commercial transport, retail sale, and storage by the end user. Not only is this precaution necessary to reduce spoilage, it minimizes pathogen growth and decreases the possibility that there would be sufficient cells to make the individual consuming the product ill. For example, improper storage led to ca. 1000-fold increase in pathogens (L. monocytogenes, Salmonella, E. coli O157:H7) when shredded romaine lettuce was subjected to 25°C for three days. The increases in pathogens occurred regardless of the composition of the atmosphere within the bag. Even when a fresh-cut romaine salad mix was subjected to five different time-temperature profiles that would be considered standard for the industry, levels of both E. coli O157:H7 and L. monocytogenes increased ca. 1000-fold. Such growth increases are cause for concern as many consumers believe that spoilage precedes any food safety risks. Another study with packaged fresh-cut salad containing romaine and iceberg lettuce demonstrated that E. coli O157:H7 growth occurred before the product’s visual quality became unacceptable.
Romaine lettuce is a hardy vegetable with a rich history dating back to at least the third millennium BCE. In Ancient Egypt, romaine lettuce was touted as an aphrodisiac and was the sacred food of Min, the Egyptian god of fertility. Romaine lettuce is used in the Maror plate during the Jewish ritual of Passover Seder. The dish symbolizes the bitterness and harshness of slavery the Jews endured in Ancient Egypt. In current times, romaine lettuce is a commonly consumed food item across the world. With its crisp texture and bitter, herby taste, it pairs well with just about any ingredient. Lettuce is predominantly used in salads but can also be grilled or sautéed. Of the 13.2 pounds of lettuce consumed per capita in 2017, 12.5 pounds can be attributed to romaine and leaf lettuces. One of the most famous romaine lettuce recipes is the Caesar salad, in which the lettuce makes up the bulk of the dish. Caesar salad is enjoyed across the globe, with each culture adding their own twist to the recipe.
Romaine lettuce is a low-calorie and low glycemic index food with 20 calories, 3 gram carbohydrates, and 2 grams protein per two-cup serving. Traditionally, lettuce has not been considered a very nutritious product, primarily because of its high water content (ca. 95%). However, nutrient composition and bioactive compounds vary among lettuce types. Romaine lettuce has nutritional benefits due to its low sodium content and its dietary contribution of fibers, folate, vitamin C, vitamin K, vitamin A, carotene, lutein, and phenolic compounds. These various phytochemical and nutrients can help support vision, blood clotting, and antioxidant activity as well as promote anti-inflammatory and antidiabetic properties.
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