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Published Research on the Sources and Spread of E. coli 0157
Author(s): Dr. Charles Benbrook
The tragic and serious outbreak of E. coli O157 infections linked to fresh spinach has focused national attention on food safety practices and polices. It has also raised hard questions about farming systems, animal husbandry and feeding practices, manure management, and the adequacy of current regulations designed to protect public health, including provisions in the National Organic Rule.
There is an enormous body of science on pathogenic E. coli that provides important clues to where this dangerous organism comes from and further steps that can be taken to keep it out of the food supply. There are over 225 serotypes of E. coli, the majority of which are not dangerous. Indeed, E. coli bacteria are essential to the healthy functioning of human and animal digestive systems. But some serotypes have picked up "pathogenicity islands" - extra genetic material that can turn a harmless bug into a dangerous threat to people and some animals. The E. coli O157:H7 serotype is among the most dangerous and heavily studied.
In the wake of the illnesses triggered by E. coli O157 on fresh spinach, many people are seeking a fuller understanding of this organism: where does it come from, how does it spread, what can farmers do to prevent future episodes?. The Center has compiled abstracts of 258 published studies on E. coli O157 to help people quickly become familiar with the range of science already published on O157. Access all abstracts in the 92-page pdf file listed below, "E. coli References." As new articles are located, this file will be updated.
Key studies drawn upon in developing answers to the FAQs are noted by the senior author's last name and year the study was published; full references can be found in the bibliography. Abstracts of the "Top 17" most useful articles from the 258-article master reference list are presented in a second pdf file (see below).
An excellent and detailed overview of pathogenic E. coli bacteria has been compiled by the University of Minnesota's Center for Infectious Disease Research and Policy (CIDRAP). It contains an overview of the various serotypes of E. coli, mechanisms of pathogenicity, and food poisoning and other disease outbreaks triggered by these bacteria..
Human Exposures to E. Coli O157
How many consumers are exposed to E. coli O157 in food?
In 1999, CDC estimated that about 73,000 people are sickened annually by E. coli O157, leading to some 2,000 hospitalizations and 60 deaths (Frenzen et al., 2005). These illnesses led to an estimated $405 million in costs, leading the authors to state "The high cost of illnesses due to O157 STEC [E. coli] infections suggests that additional efforts to control this pathogen might be warranted."
In recent years good progress has been made in reducing the number of cases triggered by E. coli O157 in ground beef. According to the most recent FoodNet data from CDC, the number of cases of E. coli O157 illnesses has declined 29% since the 1999 estimate was made. Accordingly, CDC's latest information points to about 52,000 cases of human illness in 2006. About 10% of these cases will be from produce, and about half of the 52,000 will be caused by foodborne transmission, according to other CDC studies (Rangel et al., 2005)
Beef products have been identified as the most common source of human illnesses caused by E. coli. Progress in reducing the frequency of E. coil O157 contamination in animal products, coupled with increasing frequency of illnesses linked to fresh produce, helps explain the growing concern of the food industry and regulators in the wake of the current spinach poisoning episode. Sprouts have also been implicated in a number of serious poisoning episodes. The most wide reaching episode occurred in Japan in 1996, when more than 6,300 children got sick after eating sprouts (CIDRAP review). The largest number of cases in a single episode in the U.S. was triggered by undercooked hamburgers that were served by Jack-in-the-Box restaurants in 1992-1993. This episode encompassed 501 cases and 151 hospitalizations.
In addition to exposures to E. coli O157 through food, children have been infected with the bacterium at petting zoos (Chapman et al., 2000). About 11% of the faecal samples tested for E. coli O157 at Minnesota county fairs in 2000 and 2001 tested positive (Cho et al., 2006). Contaminated drinking water, and water in lakes and pools where people swim have also triggered cases of illness linked to E. coli O157.
Sources of E. Coli O157
Where does E. coli O157 come from?
Beef and dairy cattle are by far the major source of pathogenic E. coli bacteria, including E. coli O157:H7, the specific serotype that triggered illness in the recent spinach contamination episode. During the summer in Louisiana dairy herds, 38.5% of herds and 6.5% of animals tested positive (Dunn et al., 2004). LeJeune et al. (2004) reported that 13% of 4,790 bovine faecal samples from cattle feedlots in the U.S. tested positive for E. coli O157.
A study in Louisiana concluded that deer were not a significant reservoir for E. coli O157 for cattle or humans, since only 0.3% of hunter-harvested deer tested positive (Dunn et al., 2004). A similar study in Nebraska found that only 0.25% of 1,608 samples tested positive (Renter et al., 2001).
Is it normal for cattle to have E. coli O157 in their digestive tracts?
Not really. Hancock et al. (1994) found that only 10 out of 3,570 faecal samples of dairy cattle from the Pacific Northwest tested positive for E. coil O157 in a 1994 study. They also found E. coli O157 in 10 of 1,412 samples of manure from beef cattle, just 0.71%. Several of the same scientists conducted a similar survey in 1997 and found E. coli O157 in 1% of faecal samples from beef cattle.
Duncan et al. (2000) point out in a review that "Normally E. coli is greatly outnumbered in the ruminant gut by anaerobic bacteria, producers of weak acids inhibitory to the growth of this [E. coli O157] species." Gilbert et al. (2005) found that enterohaemorrhagic E. coli [EHEC] levels were 100-times higher in cattle feed a high grain ration, compared to animals on a roughage-based diet. Herriot et al. (1998) reported that dairy heifers feed corn silage were more likely to have E. coli O157, compared to heifers not feed silage.
Dozens of published studies show that animal rations and animal husbandry play direct roles in triggering E. coli O157 colonization of the bovine digestive system (e.g., McSweeney et al., 2004; Russell et al., 2000; Diez-Gonzalez et al., 1998).
There are millions of harmless E. coli bacteria in the digestive systems of all cattle. When cows are fed high-energy, grain-based rations, the pH in their digestive systems changes to favor E. coli O157. Stress and illness can also increase the susceptibility of cattle to E. coli O157, as does holding cattle off feed (Duncan et al., 2000). Sanitary practices on the farm play a direct role in whether and how quickly E. coli O157 infections spread through a cattle herd (LeJeune et al., 2001; Scott et al., 2006; Rice et al., 2000; McGee et al., 2002).
Several studies have shown that between 5% and sometimes over 30% of cows on beef cattle ranches, in feedlots, and on diary farms in the U.S. shed E. coli O157. "Shed" means the bacteria are passed from the animal into the environment via manure.
A study focused on beef calves before they were sent to the feedlot and found that 2.5% of the animals shed E. coli O157 prior to entering the feedlot (Dunn et al., 2004).
Studies in Europe have found very little E. coli O157 in both beef cattle and dairy herds.
A study by Albihn et al. (2003) in Sweden found that just 1.2% of 3,071 faecal samples tested positive. An outbreak of human illness impacting about 100 people in Sweden in 1995 triggered the establishment of a national surveillance program testing for E. coli O157 in all cattle at slaughterhouses. A similar study in Finland found only 1.3% of dairy faecal samples testing positive for E. coli 057 (Lahti et al., 2001).
Buncic et al. (1997) tested 371 cows from 55 dairy farms in New Zealand and found only two animals shedding E. coli O157 positive manure (about one-half of one percent).
E. coli O157 was found in just two of 2,446 samples of pig manure in a Swedish study (Eriksson et al., 2003).
E. coli O157 in Beef and Dairy Cattle
Does E. coli O157 reach cattle through their feed?
Yes. Several studies have found that a few percent to over 10% of feed samples test positive for E. coli O157. In 2003 research, Davis et al. (2003) found E. coli O157 in four of 2,365 feed samples tested. Dodd et al. (2003) found E. coli O157 in 10.3% of feed samples taken from feeding troughs in Midwestern feedlots. Curiously, the Dodd study found no correlation between E. coli O157 numbers and general coliform bacteria counts. In 1998 work, Lynn et al. (1998) found no samples of feed that contained E. coli O157, despite the fact that 30% of the 209 samples tested contained other E. coli serotypes.
Can farmers do anything to reduce E. coli O157 levels in their animals?
Yes, they can do a lot. In 1998, the first study was published by Diez-Gonzalez et al. (1998) reporting that switching beef cattle in a feedlot to a high-roughage diet for the last week before slaughter triggers a dramatic decline in E. coli O157 numbers. This promising finding has been replicated multiple times and is now widely accepted in the animal health community.
Reducing E. coli O157 levels in cattle headed for slaughter significantly reduces the risk of E. coli O157 contamination on meat products, but would do relatively little to prevent the buildup of E. coli O157 in manure and manure storage lagoons. Few beef feeders have adopted the practice because of fear that a switch in diet during the last week in a feedlot may cause a drop in quality grade from Prime to Choice, or Choice to Select, and a significant loss in income. Some organic meat producers and processors encourage, or require that their producers to switch beef animals in feedlots to a high-forage diet in the last week prior to slaughter as an added food safety measure.
Garber et al. (1999) showed that dairy farms using concrete alleys and flushing systems were 8-times more likely to test positive for E. coli O157 than farmers using other manure removal systems. They also showed that E. coli levels tended to be higher in the summer than the winter.
Hutchinson et al. (2005) found that young calves still receiving milk had "significantly lower levels and prevalence of E. coli O157." E. coli pathogen levels were also reduced on farms that included some sort of bedding. Cattle on diets composed mostly of grass had less likelihood of infection with E. coli O157.
Environmental Fate and Movement
How can E. coli O157 move from cattle farms to crop fields?
Once in the environment, E. coli O157 can move in several ways around agricultural landscapes. The two most common ways are through the land application of raw, uncomposted manure, and through runoff of manure or lagoon water into streams and irrigation ditches.
Wild animals and birds can become infected, serve as a reservoir, and move E. coli O157 bacteria across a landscape, although studies assessing the importance of wildlife in transmitting E. coli O157 infections have generally concluded that wildlife plays a modest, or no role in most regions.
How long does E. coli O157 last in the environment?
This is a complicated question. E. coli O157 environmental fate is driven by many factors. In general, the bacterium lasts longer in warmer, wetter climates.
E. coli O157 is known to survive in soil for between one and six months, and sometimes longer. Many factors can extend or reduce survival in soil. Heat, lack of soil microbial activity, and moisture can extend the time period E. coli O157 survives in soil. Survival times decline in soils that have high levels of microbial activity, in cool or cold soils, and under dry conditions. Jiang et al. (2002) report that E. coli O157 lasted for 77 days in manure-amended soils at 5 degrees C, and longer than 226 days at 15 degrees C.
Incorporating manure into soils and tillage reduces survival times (Boes et al., 2005). Soils on organic farms have also been shown to accelerate the decline in E. coli levels, compared to similar soils under conventional management (Franz et al., 2005).
On the farm, E. coli O157 is known to persist in water troughs for several weeks to a few months. It can last for comparable periods in feed troughs. Transmission through water and feed troughs is considered a major source on on-farm movement from animal to animal. Berry et al. (2005) found that E. coli O157 survives in cattle feedlot soils under a wide range of manure and moisture conditions for up to 133 days.
Fenlon et al. (2000) studied the environmental fate of E. coli O157 following application of dairy slurry (liquid manure) on a clay loam soil in grass pasture. E. coli O157 was detected on the grass for only one week. There was limited transport of bacteria down into the soil (2%), and about 7% drained off the field following a rainfall event. The authors concluded that heavy rains could lead to considerable losses of E. coli O157 to leaching and surface runoff. Silage made from grass containing E. coli O157 led to a significant increase in E. coli O157 counts, under certain conditions.
Cote et al. (2005) applied pig manure to cucumber fields to track the persistence of E. coli and Salmonella bacteria. In sandy loam soils, the bacteria were undetectable after 56 to 70 days.
Entry et al. (2005) applied dairy manure and compost to potato fields and found no increase in coliform or E. coli levels after seven days. Potato skins had higher coliform and Enterococcus spp. levels following application of dairy manure, compared to composted dairy manure.
Gagliardi et al. (2002) found that E. coli persisted for 92 days on alfalfa roots in a soil microcosm study, but disappeared in as few as 25 days in fallow soils and on some crops.
How long does E. coli O157 last in raw cattle manure applied to cropland?
Survival times vary greatly as a result of soil and weather conditions. Avery et al. (2005) found that E. coli O157 bacteria were still viable in 77% of a number of organic wastes two months after land application. They concluded that storage of wastes will help reduce bacteria numbers, but cannot be counted on to totally eliminate E. coli O157.
In a study of organic and conventional lettuce production systems including applications of dairy manure spiked with E. coli O157, Franz et al. (2005) found that E. coli O157 levels declined faster in organic soils than conventional. The level of roughage in the cattle diets significantly influenced E. coli levels (the more the roughage, the lower the level).
How effective are the National Organic Program's (NOP) animal manure and compost requirements in preventing E. coli O157 contamination of farm crops?
Most scientists who have studied the impacts of manure management and application methods on E. coli survival agree that further research is needed to assure that the NOP restrictions on applying manure and compost are adequate under all conditions. NOP manure and compost restrictions are based in large part on USDA risk assessments conducted to assure the safety of human biosolid applications to conventional cropland.
The NOP rule requires compost made from animal manure to be composted in a manner that results in a temperature in the compost pile between 131 degrees F and 170 degrees F (55 to 77 degrees C) for 3 days when an in-vessel or static aerated pile system is used; or, at temperatures between 131 and 170 degrees F for 15 days using a windrow composting system, during which the rows must be turned at least five times.
Jiang et al. (2003) studied the fate of E. coli O157 during the composting of cow manure spiked with high levels of E. coli O157. They found that the pathogen became undetectable after 7 to 14 days at 50 degrees C. They recommend that compost contaminated with high levels of E. coli O157 should be held for 1 week, and preferably 2 weeks at a minimum temperature of 50 degrees C. Lung et al. (2001) found that E. coli O157 lasted only 72 hours during composting at 45 degrees C.
Ingham et al. (2004) tested the adequacy of the NOP rules in a study in Wisconsin using noncomposted diary cattle manure applied to vegetable production fields.
Within 90 days after application, E. coli levels generally had declined 1,000-fold. Levels remained detectable in enriched soils for up to 168 days. In many plots, E. coli O157 was not detected after about 100 days, leading the authors to conclude "the 120-day limit provided [in NOP rules] provided an even greater likelihood of not detecting E. coli on carrots." Still, the authors concluded that the 120-day restriction did not absolutely guarantee that all produce would be free of E. coli at harvest, especially short season produce like radishes.
Islam et al. (2004) used dairy manure and several types of compost, and irrigation water that was spiked with E. coli O157 to study persistence in the field under vegetable production systems. E. coli O157 was found to persist for 154 to 217 days and was detected on parsley and lettuce for up to 77 and 177 days after seedlings were planted.
A Norwegian research team fertilized organic lettuce with cow manure, compost, and slurry and found no difference in the bacteriologic quality of the lettuce at harvest (Johannessen et al., 2004).
Work by Mukherjee et al. (2006) in Minnesota found that the use of manure or compost aged more than 12 months on organic vegetables reduced E. coli levels by 19-fold.