S C I E N T I F I C

S T A T U S

S U M M A R Y

Foodborne Disease Significance of

Escherichia coli O157:H7
and Other Enterohemorrhagic E. coli
A PUBLICATION OF THE INSTITUTE OF FOOD TECHNOLOGISTS’ EXPERT PANEL ON FOOD SAFETY AND NUTRITION

This Scientific Status Summary addresses the virulence and disease characteristics of EHEC, their reservoirs and sources, survival and growth, and disease prevention strategies ROBERT L. BUCHANAN AND MICHAEL P. DOYLE
Author Buchanan, a Professional Member of IFT, is Research Microbiologist, Food Safety Research Unit, U.S. Dept. of Agriculture, Agricultural Research Service, 600 E. Mermaid Ln., Wyndmoor, PA 19038. Author Doyle, a Professional Member of IFT, is Director of the Center for Food Safety and Quality Enhancement, University of Georgia, Georgia Station, Griffin, GA 30223-1797 and Head of the Dept. of Food Science and Technology, University of Georgia, Athens, GA 30602.

T

he unusually virulent enterohemorrhagic strains of Escherichia coli, includ-

ing the O157:H7 serotype, have prompted food microbiologists to rewrite the rule book on food safety. These pathogens are more significant than other well-recognized foodborne pathogens for reasons including the severe consequences of infection that affect all age groups, their low infectious dose, their unusual acid tolerance, and their apparent special but inexplicable association with ruminants that are used for food. New safety recommendations for destroying enterohemorrhagic E. coli (EHEC) include cooking hamburgers thoroughly, incorporating a procedure that kills EHEC in the manufacture of raw fermented sausage, such as salami, and pasteurizing or using an equivalent processing method for apple cider. Public health problems with EHEC are being recognized throughout the world. The need for consumer education on the safe handling of foods has never been more acute.

hemolytic uremic syndrome (HUS) contained a substance that was toxic to Vero (African green monkey kidney) tissue culture cells. This verocytotoxin was produced by E. coli isolates, with O157:H7 the prominent serotype causing infection.

Enterohemorrhagic E. coli and Foodborne Illness
E. coli has been used since 1890 as a nonpathogenic indicator of enteric pathogens, such as Salmonella. However, as knowledge of enteric diseases increased, investigators began isolating strains of E. coli that had acquired virulence characteristics causing pathogenicity to humans or animals. Six classes of diarrheagenic E. coli are recognized: enterohemorrhagic (EHEC), enterotoxigenic (ETEC), enteroinvasive (EIEC), enteroaggregative (EaggEC), enteropathogenic (EPEC), and diffusely adherent (DAEC). • Definition of EHEC. EHEC are loosely defined by a combination of the symptoms they produce and the virulence factors they possess (Neill et al., 1994). The disease-defining symptom of EHEC is hemorrhagic colitis (HC), i.e., bloody diarrhea. Not all EHEC infections, however, produce overt blood in the stools. While E. coli O157:H7 infections have a high rate of bloody stools, this may not be the case for other EHEC strains. All EHEC strains produce Shiga toxin 1 (Stx1) and/or Shiga toxin 2 (Stx2), also referred to as verotoxin 1 (VT1) and verotoxin 2 (VT2). The ability to produce Shiga toxin was acquired from a bacteriophage, presumably directly or indirectly from Shigella. The toxin is a 70,000 dalton protein composed of a single A subunit (32 kDal) and five B subunits (7.7 kDal). The B subunits provide tissue specificity by binding to globotriaosylceramide (Gb3) receptors on the surface of eucaryotic cells. The A subunit has an N-glycosidase that inactivates the 28S ribosome, thus blocking protein synthesis. Endothelial cells high in Gb3 receptors are the pri-

Historical Perspective
E. coli O157:H7 (designated by its somatic, O, and flagellar, H, antigens) was first recognized as a human pathogen following two hemorrhagic colitis outbreaks in 1982 (Riley et al., 1983). The first outbreak, with 26 cases of which 19 were hospitalized, occurred in Oregon, and the second, with 21 cases and 14 hospitalizations, followed three months later in Michigan. Undercooked hamburgers from the same fast food restaurant chain were identified as the vehicle, and E. coli O157:H7 was isolated from patients and a frozen ground beef patty. Shortly after E. coli O157:H7 was determined to be a human pathogen, Karmali et al. (1983) observed that stool samples from children with

VOL. 51, NO. 10 • OCTOBER 1997

FOODTECHNOLOGY 69

respectively. Characteristic symptoms are pallor. A significant porgeographical areas non–O157:H7 serotion of HC infections are sporadic. Ground types O111:H– (H– indicates nonmobeef also has been implicated as a risk tile) and O157:H– are more common factor in those sporadic infections (Le in Australia (Goldwater and BettelSaux et al.g. Although the symptoms of E. EHEC require the presence of other virulence markers. HUS) ever.. and in other ed States (CDC. Approximately 15% of cases 70 al. O104:H21. An AustraO4:H–. 1995. This condition resembles HUS except that it generally causes less renal damage...... E. 1995). cur (Siegler et al. coli O157:H7 infections are distinctive. has significant neurological involvement. O45:H2. Other and its primary complications (hemolytic uremic EHEC serotypes. This has led to classification of EHEC largely on the basis of Fig. and from consumption of contaminated O145:H– (Beutin et al. Fig. Great Britain. HUS is the most common. HUS occurs most often in children under the age of 10. the presence of a plasmid-encoded enterohemolysin is characteristic of EHEC. 1995). 51. and regions in Europe. lack of urine formation (oligo-anuria). coli O157:H7 has been implicated in outbreaks worldwide and is the primary cause of HC and HUS in the United States. and a high incidence of Dry-cured salami was associated sorbitol-positive (capable of fermentwith an E. Pai et al. 1991). intravascular destruction of red blood cells (microangiopathic hemolytic anemia). 1988). • Disease Characteristics. Insulin-dependent diabreaks. e. types predominate. is not sufficient to make E. depressed platelet counts (thrombocytopenia). 1993). they may be confused at any single phase with other diseases or conditions (Tarr. pancreatitis. colonic perforation. seizures. NO. accounting for the toxin’s affinity for the colon and the renal glomeruli. Tzipori et OCTOBER 1997 • VOL. though longer periods (3–5 days) have been reported. coli O157:H7 C O N T I N U E D mary target. coma. 1—Symptoms and time course of Eschercharacteristics of seroichia coli O157:H7 infection (hemorrhagic colitis) type O157:H7. and hypertension. nonbloody diarrhea that may be followed by a period of “crampy” abdominal pain and short-lived fever. lead to early development of chronic • Foods Implicated in EHEC Outkidney failure. is ubiquitous among EHEC strains. heim. 1996). however. Toxin alone. The eae chromosomal gene. 1). The toxin can also indirectly damage cells by releasing cytokines. encoding for an outer membrane protein associated with attachment. • Serotypes included in EHEC. stx-positive isolates are isolated frequently from humans. and strokes. Large outbreaks include the A second complication associated 1992–93 outbreak that affected more with E. coli pathogenic. Since 1982. stroke. swelling (edema). For example. 1988). 1994. fermented meats and cause Other serotypes of EHEC strains are illness (Tilden et al. 10 FOODTECHNOLOGY . coli O157:H7 outbreak in the ing sorbitol-containing culture mediwestern United States. coli O157:H7 is thrombotic thrombocytopenic purpura. lian outbreak of HC and HUS resulted O103:H2. O111:H8.e. and acute renal failure. 1995). Several life-threatening complications may occur in HC patients. Canada. central nervous system deterioration. O11:H–. for example. The pathogen is likely responsible for 85–95% of HUS cases (Griffin. Approximately half of HUS patients require dialysis. seronot associated with outbreaks. and the mortality rate is 3–5%. most often associated with outbreaks in A small number of HUS cases may rethe United States (Griffin and Tauxe.to 10day phase of overtly bloody diarrhea accompanied by severe abdominal pain and moderate dehydration. 1993). Ground beef has been the food betes may also persist in HUS patients.. The initial diarrhea increases in intensity during the next 24–48 hr to a 4. such as tumor necrosis factor. associated with HC and HUS. Other HUS-associated complications may include seizures. apparently nonpathogenic. and is restricted primarily to adults (Boyce et al. The onset of HUS is approximately a week after the onset of gastrointestinal symptoms. The initial symptoms of HC generally occur 1–2 days after eating contaminated food.. demonstrating um) O157:H– in central Europe has that low levels of this organism can surbeen reported (Bitzan et al. howsyndrome. To be fully pathogenic. Symptoms start with mild.. 1993. i. O26:H11. Although its role is unclear. 1993).. vive in acidic.S C I E N T I F I C S T A T U S S U M M A R Y E. are reported occathan 500 individuals in the western Unitsionally in these regions.

It has been suggested that outbreak–associated strains of E. 1997. Unpasteurized apple juice and cider have received considerable attention due to local and multistate outbreaks (Besser et al. but not in most. coli O157:H7 did not form atvaries widely. 1991) or animal-to-person (Wilson et al.881 feedlot cattle were positive for antibodies to the O157 antigenic lipoE. coli O157:H7. from 104 to 106 CFU/g after 48 hr of healthy ewes revealed that fecal shedto 5–102 CFU/g at 14 days). 1993). The infectious dose (2–2. results revealed that: Deer and cattle fecal samples obtained • E. coli O157:H7.. NO. several and persistence of weeks to months infection in herds. 1994).. 51.. 1993).. coli Stx1 (Johnson et al. coli suspected of being associated have established O157:H7 with indiswith Escherichia coli O157:H7 that deer are a tinguishable pulsed outbreaks source of the field gel electropathogen and that phoresis (PFGE) getransmission of nomic DNA profiles Undercooked ground beef the pathogen may can be isolated from Raw milk occur between calves in different Unpasteurized apple juice/cider deer and cattle states or farms Dry cured salami (Keene et al. but a nonspecific association has often been made with the consumption of food in restaurants (Waters et al. • Reported incidence among cattle • E. coli O157:H7 is confined to the seasonal..6%) prompt and sustained increases in serum of 11.. coli O157:H7 with undercooked ground beef and raw milk led to investigations of the role of cattle as a reservoir of the pathogen. (Faith et al. occurred in Japan in 1996. late (Rice et al.. O157:H7 to persist in and reinfect cattle • Fecal shedding of E. Recent Cray and Moon. Other foods have been associated with EHEC outbreaks worldwide (Table 1). coli O157:H7 that have a strong immune response is frequently is intermittent and of short likely to contribute to the introduction duration. 5. mals. spiral colon. alfalfa sprouts ing contaminated lated from feces of Yogurt venison jerky. The ability of E. omasum. for detecting E. 1996). most do not possess the other virulence determinants associated with fully pathogenic EHEC. do not correlate • E. coli O157:H7 have been identified: Cattle..2%) of 965 dairy calves (Zhao et al. tion. with 31% of sheep positive in gastrointestinal tract. 1997. which are often foci for infections (Belongia et al. leftover jerky.S.. and none achs (rumen. coli O157:H7 may have enhanced acid tolerance (Buchanan and Edelson. were isolated Meng et al.. E. This outbreak and a second one a year later were associated with radish sprouts..e. 1995).. surveys with 1010 E.. The inability of E. coli isolates capable of producing one or more Shiga toxins can be isolated readily from meat. 1994. A six-month study (e. i.4% of polysaccharide and to a lesser extent to feedlot cattle were positive for E. which caused thousands of illnesses. however.. An additional 0. For exam• More than one Produce from manure-fertilized garden ple.. coli substantially among positive herds O157:H7 shed in the feces of some ani(Hancock et al.. coli the same deer. coli O157:H7 is not pathogenic to from a ranch in Texas had the same Shicalves. Several surveys of fecal shedding of E. The association of E. and reticulum) in November. coli O157:H7 Sheep. Sources are not identified in a substantial portion of EHEC cases. Oral inoculation of calves and steers • Results of two major U. cal responses.. 1995). E. 1996). • The numbers of E. with the forestomJune. 1995). inoculation with 1010 CFU did ga toxin-producing E.. the same animal or coli O157:H7 with different animals Sandwiches the same distincwithin the same herd Water tive PFGE profile (Faith et al.. For example. ding of the pathogen was transient and • E... E. 1996). 1995). coli O157:H7 outbreaks has been consistently low—a characteristic associated with the organism’s acid tolerance. and fragments of the deer hide. dling practices implicated or investigations • Strains of E. This may be attributed in part to secondary person-to-person (Griffin and Tauxe. coli O157:H7 1995). however. 1993).. Sheep have also been identished in feces decreased dramatically durfied as a reservoir of E. S T A T U S S U M M A R Y Reservoirs and Sources of E. coli Handling potatoes outbreak involvO157:H7 can be isoRadish sprouts. from the human Calves have been cases. coli O157:H7 Several reservoirs and sources of E. EHEC isolates of serotypes O111:H– and O157:H– were isolated from both patients and product (Paton et al. Zhao et al. Deer.S C I E N T I F I C mettwurst (CDC. in part because of differtaching and effacing lesions and did not ences in sensitivity of procedures used colonize mucosal surfaces. coli O157:H7 outbreak. and seafoods (Samadpour et al. 1997. The largest reported E. coli VOL.S. however. coli O157:H7 to ferment sorbitol. Meng et al. 1982). poultry. 1995). Alfalfa sprouts were also implicated in a recent outbreak in the U. • Prevalence of fecal excretion varies • Fasting increases the levels of E.. coli O157:H7 produced the following general observations: • Young animals tend to carry E.. The sheep showed no signs and distal sites (distal ileum.7% positive in August. (Brown et al.. coli O157:H7 is similar to Shigella in its association with day-care centers. A 1980 outbreak of HUS involving fresh apple juice is now suspected of being caused by EHEC (Steele et al. coli (Zhao et al. proximal FOODTECHNOLOGY 71 . Table 1 Foods or food hanE. coli O157:H7 levels in calf feces with elimination of carriage by cattle or range from <102 CFU/g to 105 CFU/g protection of calves against reinfection by the same strain. 10 • OCTOBER 1997 cecum. 1995). 1996) spread of EHEC. Moon.000 cells) associated with foodborne E. The serologiO157:H– (USDA/APHIS. uncooked meat from experimentally infected with E. Cray and carcass. Rice et al. coli O157:H7 ing the first 14 days postinoculation (Kudva et al. Lettuce 1995). 1995). coli O157:H7 induced indicated that 31 (3. coli O157:H7 isonot induce significant clinical disease. and descending coO157:H7 more frequently than adults lon) being the principal sites of localiza(Zhao et al. 1995) and 191 (1. is not associated with its virulence (Fratamico et al. 1996).g. 1996. 1994). 1996. a saw used to cut up the O157:H7 (Brown et al. 1995).. 1995). in a recent strain of E.

1996). The minimum pH for E.. Leyer et al. compared to 10–31 days at 8°C (Zhao et al.. 1995). coli O157:H7 was acetic > lactic ≥ citric. Survival in these foods is extended greatly when stored at refrigeration temperature. Animals perorally administered 109 E. above 44°C (Doyle and Schoeni. coli cells in the stationary phase of growth are substantially more acid tolerant than cells in the exponential phase. In 1991.5. 1995). EHEC strains can have a high degree of acid tolerance. They compared the effects of mannitol. 51. The effect of temperature on the growth rates of both E. The minimum growth temperature for E.. 21 cases of E. 1996). This increased tolerance is associated with expression of genes regulated by the rpoS sigma factor operon (Cheville et al. and water activity. 1992). Mo. A large outbreak of 243 cases including four deaths was associated with contamination of municipal water in Cabool. NO. coli O157:H7 focused primarily on the effect of sodium chloride. the relative inhibitory activity of organic acids on E. have also been identified. Acid tolerance in E. Many O157:H7 isolates. surviving virtually unchanged during 2. and NaNO2 on the growth kinetics of E. (1995) found that the upper temperature for E. 1994). Induction of acid tolerance in E. coli O157:H7. ingested fecally contaminated lake water. oxidase-negative. 1996). and found that all three contribute to the microorganism’s overall acid tolerance. since several outbreaks have been associated with low levels of E. When the pH falls below the minimum for growth. coli) broth at 44. water activity. An acid tolerant state can persist for extended periods (≥28 days) if the cells are stored at refrigeration temperature. A shedding sheep passed E. radiation. from December 1989 to January 1990 (Swerdlow et al. The induction of acid tolerance can also enhance the organism’s ability to survive other stresses. The pathogen has been shown experimentally to survive for several weeks to months in a variety of acidic foods. For example.e. 10 Factors Affecting Survival and Growth Like all bacteria. and mathematical models have been developed to describe how temperature interacts with pH. pH. Ore. 1995). including mayonnaise (Zhao and Doyle.. sheep apparently negative for E. coli O157:H7 infection (Doyle et al. coli is a complex phenomenon. i. however. coli O157:H7 began to shed the bacteria when the animals were removed from confinement and their feed was changed from alfalfa pellets to sage brush and bunchgrass (Kudva et al. Palumbo et al.5 and 7. acid-tolerant. 1985. coli. (1996) examined three mechanisms of acid resistance. for example. all strains grew in BHI (brain heart infusion) broth at 45°C.. Studies on the effect of water activity on the survival and growth of E. 1995). The pathogen’s survival in acidic foods is particularly important. E. with the exception of isolates of serotype O157:H7. Two large water mains. pH. coli growth is 4. coli O157:H7 behaves similarly to other E... E. E. (1993) reported that in beef slurries.0%) with temperature. Bathers.5–5. Buchanan and Bagi (1994) developed a mathematical model for the effects and interactions of NaCl concentration (0.g. 1996. broken because of extreme cold weather.S C I E N T I F I C S T A T U S S U M M A R Y E. organic vs inorganic) and acid concentration influence the effect of pH on E. Acid-sensitive EHEC strains. so this is not a characteristic unique to pathogenic isolates. The type of acid (e. 1994). 1996).. Buchanan and Edelson.. Abdul-Raouf et al. coli O157:H7 populations decline over time. Growth rates are similar at pH values between 5. sorbitol. coli O157:H7 to a non-dosed pen mate..5 and 37°C (Benjamin and Datta. 1993). Rowbury. (Keene et al. if at all. coli biotype 1 and EHEC has been determined.. the pathogen survived in apple cider for only 2–3 days at 25°C. additional stresses raise the minimum pH for growth. coli are differentiated from other Enterobacteriaceae (family of Gram-negative. and sucrose as humectants and concluded that while humectant differences OCTOBER 1997 • VOL.. and sodium nitrite to affect growth kinetics (Buchanan and Bagi. oxidative. E.to 7-hr exposures at pH 2.. This is dependent on the interaction of pH with other growth parameters. and glutamate-dependent. 1996.. 1994. 1995.5 (Buchanan and Bagi. Rajkowski and Marmer. coli O157:H7 fecally shed the bacteria for up to 92 days. and Cheddar cheese (Reitsma and Henning. but six of sixteen strains did not grow in EC broth. E. 1994). 1993). both growth phase–dependent and inducible. coli also possesses an inducible alkali tolerance response (Rowbury et al. um–dependent. 1992). though. but decline rapidly at lower pH values (Buchanan and Klawitter. and antimicrobials (Rowbury. facultatively anaerobic rods) on the basis of their ability to grow and produce gas in EC (E. presumably. • Temperature. • pH. 1997). the survival and growth of E. coli O157:H7 C O N T I N U E D of disease throughout the study. coli O157:H7 under otherwise optimal conditions is approximately 8–10°C (Buchanan and Bagi. coli O157:H7 among cattle (Faith et al. Lin et al. 1995). non-enterohemorrhagic strains have also been identified. and apple juice. EHEC strains respond to temperature in the same manner as non-EHEC strains. coli growth. including many toddlers not yet toilet trained. apple cider (Zhao et al. however. 1995. Gill and Phillips. • Water Activity. coli O157:H7. 1984). arginine-dependent. Recent studies have indicated that induction of acid tolerance also increases the microorganism’s resistance to heating. sausages (Clavero and Beuchat. Drinking and recreational waters have been vehicles of several outbreaks of E. Conversely. apple cider.5°C. such as fermented sausages.0–4. coli O157:H7 in foods are dependent on the interaction of various intrinsic and extrinsic factors such as temperature. Water has been suggested as a vehicle of transmitting E. Water. 1994. Sutherland et al. catalase-positive. coli O157:H7 growth was culture medi72 FOODTECHNOLOGY .. Small et al. and new in-ground water meters may have contributed to the outbreak. do not grow well. 1996). coli O157:H7 surviving in acidic foods. Diet influenced fecal shedding of E.. coli can enhance its survival in acidic foods (Cheville et al. 1994). coli O157:H7 infection were traced to swimming at a lakeside park in Portland.

and consumption of the final products that would have to be considered in a farmto-table HACCP plan. verification based on microbiological analysis would have to depend on the use of an appropriate indicator organism that could provide a measure of how well a process controls factors associated with risk of E. In such instances.. it is assumed that the ultimate source of E. 1994. Model system studies on the microorganism’s ability to survive acids and other agents at non- Disease Prevention E. coli O157:H7 to beef carcasses (Dickson. fermented sausages. innovative approaches FOODTECHNOLOGY 73 . Trisodium phosphate has been evaluated as a sanitizing agent for carcass surfaces and equipment. coli O157:H7 cells that have been removed from carcass surfaces by rinses with sanitizing agents is still unclear. Two approaches that have potential are competitive exclusion and vaccination. possibly due to difficulty in removing E.. coli O157:H7 from equipment surfaces (Somers et al. 1992)... the low incidence of E. EHEC. Growing E. 1992). 51. Various alternatives to trimming have been investigated for the removal of enteric pathogens. The HACCP plan listed skinning. coli O157:H7 on carcasses is fecal contamination during animal production and slaughter operations. This reduces the critical control points to assuring the effectiveness of that step and preventing subsequent cross contamination. • Farms. 1995). coli O157:H7 represents unique challenges to preventing foodborne disease. 1994). marketing. For example.g. apple cider). 1994. This approach uses defined bacterial cultures that can greatly reduce colonization of Campylobacter jejuni in poultry (Schoeni and Doyle. and cattle exposed to E. NO. there is one or more critical control points associated with steps that either reduce the likelihood that the pathogen has gained access to the product or actively reduce (but not eliminate) the levels that may be present. particularly at refrigeration temperature (Bagi and Buchanan. However. Hence. the committee identified factors associated with animal production practices and with the distribution. Like other E. Typically. Investigators found that acid rinses had little effect on eliminating E. 1993).98 (Buchanan and Bagi. Competitive exclusion involves the use of microbial cultures that out-compete pathogens from colonizing specific niches. coli O157:H7 from the surface of beef tissues (Brackett et al. Recent observations showed that E. coli O157:H7 can survive for many weeks when desiccated. Several investigators observed differences in the effectiveness of acid treatments between lean and fat tissue and among different portions of the carcasses (Cutter and Siragusa. 1997). coli O157:H7 as a hazard. Cray and Moon. coli O157:H7 does not appear to have any increased resistance to antimicrobial food additives. Traditional trimming procedures can reduce E. 1996. since the focus is on risk reduction instead of risk elimination. a slightly greater effect was observed on fat tissue (Dickson. 1996). • HACCP. S T A T U S S U M M A R Y will be needed for vaccines to be effective. 1995). An important component of HACCP application in animal production is reducing the carriage of E. pose some unique problems when developing and implementing HACCP plans. Since such processes cannot assure complete absence of the pathogen. 1996). evisceration. The Hazard Analysis and Critical Control Point (HACCP) system continues to be the most effective means for systematically developing food safety protocols that can reduce the risk of EHEC infections. fermented meats). coli O157:H7. coli O157:H7 levels on areas of the carcass with visible fecal contamination (Hardin et al. coli O157:H7 in foods makes direct microbiological testing for the pathogen as a means of verifying the effectiveness of a HACCP program of limited benefit. 1991). the generic HACCP plan for beef slaughter and fabrication developed by the National Advisory Committee on Microbiological Criteria for Foods (NACMCF. coli O157:H7 contamination. Its low infectious dose in combination with the disease severity means that successful prevention strategies must focus on reducing or eliminating the presence of the microorganism. coli. HACCP plans that do not include a step that kills pathogens are more complex. 1995). coli at elevated levels of NaCl induces rpoS expression with associated increases in thermotolerance and H2O2 resistance (Hengge-Aronis et al. there will also be critical control points associated with preventing pathogen growth. In addition to these specific activities associated with slaughter.. • Slaughterhouse. final bactericidal rinse. Fecal contamination is associated primarily with contamination of the carcass during hide removal and spreading of contamination to other carcasses by equipment and workers’ hands (Dickson and Anderson. ground beef) or ready-to-eat products that do not receive a definitive treatment that assures elimination of E. For example. coli O157:H7 are not protected from reinfection (Johnson et al. Recent studies with E.g... Preevisceration washing decreased the subsequent attachment of E. 1997. Fratamico et al. Fratamico et al. 1996).. Hardin et al. For products that depend on nonthermal interventions to assure product safety (e. The actual fate of E. but a substantial effect on fat tissue. however. post-skinning rinsing/ bactericidal spray. Its overall effectiveness. chilling. • Antimicrobials. coli O157:H7 (e. 1993). coli O157:H7 suggest that rinsing of carcass surfaces with solutions of organic acids may have limited effectiveness. coli O157:H7 on lean tissue. was similar to that achieved with organic acids (Fratamico et al. Most desirable is a process that includes a step lethal to the pathogen. rather than on preventing pathogen growth.. Spray chilling with 1– 2% acetic acid only produced a 1-log cycle (tenfold) reduction of E. coli O157:H7 by animals.S C I E N T I F I C occur at limiting aW values. differences among humectants were minimal at aW 0.. as is done in more traditional approaches. coli O157:H7 from beef surfaces previously chilled (Hardin et al. coli O157:H7 does not form attaching and effacing lesions or colonize mucosal surfaces of the gastrointestinal tract (Brown et al.g. 1993) included E. 10 • OCTOBER 1997 the desired level of inactivation may be a necessary part of the hazard analysis phase of HACCP implementation. 1995).. Holding the meat for 24 hr indicated only a small residual effect on lean. and maintenance of refrigeration as likely critical control points. Vaccination involves exposing an animal to an attenuated pathogen or an antigen of a virulent microorganism to produce immunity. due to its high pH. validation that the integrated process can achieve VOL.. This focus is particularly important for raw products that may not be thoroughly cooked before consumption (e. traditional vaccination approaches are not likely to be successful with E. Trisodium phosphate can increase the removal of E. 1995).. E. E..

(1995) estimated that the D60°C for E. 1992) and Cheddar cheese (Reitsma and Henning.. coli O157:H7 in fruit juices. coli O157:H7 in apple juice (pH 4. NO. For example. Line et al. Prior heat shock increases thermal resistance. and radiation pasteurization doses of 1. One that has potential. particularly for meat and poultry products.. Modified-atmosphere packaging. thermal resistance is more strongly influenced by fat content. prevention of cross contamination between raw and cooked foods.0) was 0. 1993). coli O157:H7 (Abdul-Raouf et al. The organism is inactivated readily by pasteurization of milk. however. E. D-values (decimal reduction time. Doyle and Schoeni. coli O157:H7 strains have been shown to grow on many vegetables if stored at temperatures that support growth (Abdul-Raouf et al.. unpublished data) indicate that low-dose irradiation of apple cider is effective. While food processing research with E.4 min. 1993). an increasing number of outbreaks have involved fruits and vegetables. and food scientists have made great strides in understanding E. coli O157:H7 in dairy products. reported D60°C values for serotype O157:H7 in ground products range from 0. Radiation inactivation is temperature dependent. Infected food handlers could potentially serve as foci for E. and appropriate refrigerated storage are key factors for reducing the risks associated with E. the higher the fat content. used extensively with produce. however. Drink only pasteurized milk and apple juice. There appears to be little data on the ability of irradiation to control E. coli O157:H7 (Teo et al.. the greater the thermal resistance. and steam pasteurization cabinets are used for whole carcass treatments. 6. higher doses are required when ground beef is irradiated at frozen temperatures. coli O157:H7 while maintaining the raw character of the animal tissue is a new method for reducing the presence of enteric pathogens on meats and poultry. coli O157:H7. particularly during the first 48 hr of an infection when symptoms are still relatively mild or in those individuals who do not have overtly bloody stools. Thayer and Boyd. 10 FOODTECHNOLOGY . Cells held at refrigeration are more sensitive than cells heated directly 74 Table 2 Recommendations to reduce the risk of acquiring an Escherichia coli O157:H7 infection 1. coli O157:H7. 1984. The pathogen persisted during the manufacture of cottage cheese (Arocha et al. The use of steam to briefly heat carcass surfaces to temperatures sufficient to inactivate E. Outbreaks associated with raw milk have prompted investigations into the fate of E. i. coli O157:H7 can be controlled readily through traditional thermal processing techniques. though recent studies (Buchanan et al. molecular biologists. does not prevent the growth of E.. coli O157:H7 has concentrated on products of animal origin.. 1996).8 min. coli O157:H7 infections. from the frozen state (Jackson et al.e... Wash hands thoroughly after changing diapers or after providing care to children or adults suffering from a diarrheal disease. is ionizing radiation. Wash hands thoroughly after handling animals.. pasteurization would be expected to control E. E. deer. 5. Undercooking has been an important contributing factor in E. Summary It is apparent that microbiologists. Wash fresh fruits and vegetables thoroughly before eating. coli O157:H7 on fruits and vegetables. The pathogen is relatively radiation sensitive. coli O157:H7 while maintaining the raw character of foods are currently being investigated.000-fold) reduction of E. and anaerobic incubation increases recovery of heated cells (Murano and Pierson. coli O157:H7 infections and conversely play an important part in their prevention. adequate cooking temperatures and times. 1995.S C I E N T I F I C S T A T U S S U M M A R Y E. Elevated pH values (pH 10–11) can enhance the thermal destruction of E. Splittstoesser et al. Dairy pasteurization processes designed to kill Coxiella burnetti should be sufficient to eliminate E. or dogs. Food handling and preparation practices can contribute to E. 1996). or the time required to destroy 90% of the population) have been determined at a number of different temperatures in various ground meat and poultry products (Ahmed et al. • Home and Foodservice. and levels declined during aging of the Cheddar cheese. Avoid swimming in lakes or ponds used by cattle and drinking surface water that has not been properly treated to eliminate pathogens.. The steam vacuum system is reportedly capable of achieving a 5-log cycle (100.5–3. goats. Hao and Brackett. 3. Steam vacuum systems are used for spot removal. 4. particularly cattle. 51. D-values vary to some degree among ground products. 1993). coli O157:H7 on inoculated beef surfaces (Dorsa et al. coli O157:H7 outbreaks associated with ground beef.4 to 0. In particular. • Food Processing. 1993). Do not use fresh manure from ruminants to fertilize vegetables or fruits. 1994. 2. coli O157:H7 C O N T I N U E D lethal temperatures indicate that the exposure times associated with carcass sanitizing are too short to achieve any significant direct inactivation and suggest that the primary effect is the physical removal of the microorganisms. the organism’s low infectious dose requires that processing be sufficient to assure a low probability of the pathogen’s surviving. Alternative technologies to thermal processing that could eliminate or control E. 1993.0 kGy appear to be sufficient to eliminate it at the levels that they are likely to occur at in ground beef (Clavero et al. coli O157:H7 infection (Table 2). 1996) made from inoculated milk.. Cook ground beef and venison thoroughly (minimum 160°F) before eating. coli O157:H7 and related EHEC and OCTOBER 1997 • VOL. 1995). 1991). Similarly. 7. Adherence to good food handling practices recommended for foodservice and home preparation represent the last line of defense for assuring prevention of E.

Rev. Med. 1996. Cutter. Lee..K. P. I. Griffin. J. and Siragusa. M.P. Balan. J.R. 1994.W.W. Food Protect. K. U. 61: 1669–1672. Harmon. Escheri- References Abdul-Raouf. heat. and Schoeni.M. D. Osterholm. Environ. Clavero. R.M. D. Microbiol.Y. Acuff. D. Cheng. 1996. M. Buchanan.V. Environ.T. and Beuchat.D. Henneberg. Appl...-S. Ammend.. Epidemiol. Food Protect. Food Protect. J. Buchanan. 64: 1879–1883. M. salmonellae.H. M.T. Assn. and Bettelheim.L. Microbiol. H.C.. Bagi. Dickson. P. J.. J. R. 1993.E. Blaser. Appl. Tarr. 1995. Beuchat. 10 • OCTOBER 1997 FOODTECHNOLOGY 75 . Susceptibility of preevisceration washed beef carcasses to contamination by Escherichia coli O157:H7 and salmonellae.N. 1992–1993... M. a key lesson dramatically reinforced by the emergence of E.S. 269: 2217–2220. H. R. M.E. Food Microbiol. Zhao.. M. Belongia. P.L.. L. R.. D. Mortal. Microbiol.. 1993. Appl. 1995.. C. Appl. 1991. 183: 13–21.A. The epidemiology of infections caused by Escherichia coli O157:H7. Addressing these questions will require the continued effort and support of basic and applied scientists from a variety of disciplines. J. J.P. T. J. Immun. and Brackett. 1997. Environ.. The effect of media composition on the relationship between temperature and growth rate of Escherichia coli.” ed.. Microbiological decontamination of food animal carcasses by washing and sanitizing systems: A review. Goldwater. J.N. S. J. Buren. Fratamico. M.K. Buchanan..N. 1997.L.A. Beuchat.. 1996. 1993.G. W.. Petric. water activity. and Datta.G.. M. and sodium chloride on the growth kinetics of Escherichia coli O157:H7. Microbiol. 17: 37–39. J.M. Microbiol.. 1994. Benedict. P.G. J.M. Listeria monocytogenes. and Johnson.S. The role of Escherichia coli infections in the classical (enteropathogenic) hemolytic uraemic syndrome: Results of a central European.G. Dis. J. K. P.H. Med. 23: 61–63. E.. K. P. J. 277: 1229–1231. 56: 191–193. J.H. Aleksic. J.W.D.. Dickson. Environ. J.K. Weekly Rept.. Hatfield.C. Culturing enterohemorrhagic Escherichia coli in the presence and absence of glucose as a simple means of evaluating the acid tolerance of stationary-phase cells..D. Environ... Am. and Griffin. 333: 364–368. and Fischer. and Kaspar. A swimming-associated outbreak of hemorrhagic colitis caused by Escherichia coli O157:H7 and Shigella sonnei.. T. M. Cheville. Am.M. 59: 230–237. C. J. pp. Lett.P. Keene. multicenter study. 175: 259–265. C. Environ.A. CDC. Arnold. Factors influencing attachment of Escherichia coli O157:H7 to beef tissues and removal using selected sanitizing rinses. Y. and Anderson. 331:579–584. Microbiol. L.S.D. and Tauxe. Update: Multistate outbreak of Escherichia coli O157:H7 infections from hamburgers—western United States. 1992. Besser.L.R. Heat-resistance of Escherichia coli O157:H7 in meat and poultry as affected by product composition. R. M. Epidemiol. R. other enterohemorrhagic E. Med. Microbiol. Appl. B.L.J. D. T.D. Keene. Food Sci. 62: 1822–1824. Outbreak of Escherichia coli O157:H7 infections traced to jerky made from deer meat..R. Doyle. Heat resistance of Escherichia coli O157:H7 in a nutrient medium and in ground beef patties as influenced by storage and holding temperatures.G. Intl. W.. (In press). Microbiol.I. and temperature and suitability of media for its recovery. Virulence factors and phenotypical traits of verotoxigenic strains of Escherichia coli isolated from human patients in Germany. G.. 1995. 1994. E. A. and Bagi.T. Food Microbiol. Doyle. Doyle.M. J. I.. 1992. G..D.. K. Preservation of Listeria monocytogenes and other pathogenic foodborne bacteria on silica gel. 1985... Microbiol. and Moon. Microbiol.R. J..P.. C. Control of Salmonella typhimurium. Rupnow. In “Food Microbiology: Fundamentals and Frontiers... Ahmed. W. P. J. J. 1997.E. S T A T U S S U M M A R Y and T. M. P.G. 60: 2069–2075. Environ.. Fratamico. Lett. M. Lucia. however. pp. W. Comparison of methods for decontamination from beef carcass surfaces. M.. Lancet i: 619–620. Epidemiol.H. A... R. 44: 550–551.P. 59: 4245–4252.J. and Zhao. Infect. 58: 368–374. and salt tolerance in Escherichia coli O157:H7. Wells.L. Luchansky. 1995. 57: 97–103. Barrett. Food Microbiol.I.. rpoS regulation of acid.A. Atlanta. 1993.S. C. P. 1995. Hoesley. Weber.R. and Brackett. S. D. S.E. Effect of diet on the shedding of Escherichia coli O157:H7 in a sheep model. R. Benjamin. CDC. Karmali. 55: 133–140. and Ammar.A. 62: 4009–4013. P. 62: 2735–2740. 1994.M. 57: 198– 203. Schultz. Jackson.. Appl. Centers for Disease Control and Prevention. and Siragusa.. and Doyle.E. M. S. G. Experimental infection of calves and adult cattle with Escherichia coli O157:H7..S.. Prevalence and clonal nature of Escherichia coli O157:H7 on dairy farms in Wisconsin. 171–191.. Dickson. Pfaller. Community outbreak of hemolytic uremic syndrome attributable to Escherichia coli O111:NM— South Australia. Zhao. Lett. T. New York. Food Protect. D. L.” ed. D.M. Microbiol.R. Hancock. and Savell. 2: 285–290. Centers for Disease Control and Prevention. Kinsel. 19: 2–4. N.S C I E N T I F I C developing means for controlling them in foods. Continued vigilance and the ability to rapidly mobilize research capabilities must be an integral part of food safety programs if we are going to minimize the impact of new foodborne microbial threats to human health. coli.... Brosch. Y.R. Braun. Appl. M. Survival and growth of Escherichia coli O157:H7 on salad vegetables.. Cutter. Ineffec- tiveness of hot acid sprays to decontaminate Escherichia coli O157:H7 on beef. and Fleming. C. Meng.. Ansay. Food Microbiol. 61: 1363– 1370. L.E.. Food Sci. T.. C.J. Serum antibody responses of cattle following experimental infection with Escherichia coli O157:H7. Effectiveness of a steam–vacuum sanitizer for reducing Escherichia coli O157:H7 inoculated to beef carcass surface tissue. Besser. L.. N. G. and Acuff. Hao. R... R. Appl.W. and Klawitter. 1996. Clavero. J. J.A.. Acid tolerance of enterohemorrhagic Escherichia coli. Med.M. Morb. Environ. Food Protect. Escherichia coli O157:H7 and the hemolytic uremic syndrome. The prevalence of Escherichia coli O157:H7 in dairy and beef cattle in Washington state. 56: 330–332.J.K. T.G.. K. Assn. 1995..H. R. 1993. 9: 185–196.. 59:1999–2006. Transmission of Escherichia coli O157:H7 infection in Minnesota child day-care facilities. R. Brown. 1993. 61: 1586–1590. Mortal. Survival and growth characteristics of Escherichia coli associated with hemorrhagic colitis. Hardin. 1996. Engl. and Lim. Lange.. J. Ravdin. NO..G. initial pH. Buchanan.-Y. Rice.. 13: 60–98. Doyle. In “Infections of the Gastrointestinal Tract..L. Buchrieser. Assn. J. J.M. 1995.R. S. 51. Buchanan. P. Appl. 1984.. and Phillips. 62: 1519–1525. S. L. Williams. 1994. We cannot take for granted that foods and food practices that have been traditionally safe will remain that way in the future.E.P. and Cooke. Brackett. 60: 606–610. Food Protect. Lidwig. and Huffman. and Cooke.E. Environ. C. It is also evident. The effect of incubation temperature. Faith.M. 1992.A. and Doyle. C. Weekly Rept. 1995. Intell. Shere. Appl.. R. H. P.L. Beutin. Hardin. Appl. L. 1993.. McAnulty. M. Montville. Oxman. and Kaspar. Jr. and Paros. 58: 1065–1068.E.B..P. McVey.. L.. Efficacy of organic acids against Escherichia coli O157:H7 attached to beef carcass tissue using a pilot scale model carcass washer.. and Hovde. and Campylobacter jejuni in raw ground beef by gamma irradiation.. Zhao.M.C. Dorsa. 1996. D. N.R. Appl. 1983. 63: 27–32. Med. Environ. C. Washington. 1997.P. Virulence of an Escherichia coli O157:H7 sorbitol-positive mutant. B.T. Microbiol.. N. and Hovde. 1991. G. Johnson.J. Monk. that there are major scientific questions that must be answered before we will be able to fully assess and manage public health concerns associated with their foodborne transmission.. Behavior of hemorrhagic Escherichia coli O157:H7 during the manufacture of cottage cheese. J. Morb. Commun..T. Boyce. J. Kudva.L. On a broader front. Immunol. L. Microbiol. and Escherichia coli O157:H7 on beef in a model spray chilling system. coli O157:H7 is that both the macroscopic and microscopic worlds change continually. and Gleier. Survival of Escherichia coli O157:H7 in broth and processed salami as influenced by pH. S. Food Protect.. Escherichia coli O157:H7 and other enterohemorrhagic Escherichia coli. Rice.R. K. and Bullerman. Doyle. R. J.. Bacteriol. M. Griffin. and MacDonald.. ASM Press. M. S. and Doyle. Infect. Atlanta.. L. Arnold. Hatfield. The role of enterohemorrhagic Escherichia coli serotypes other than O157:H7 as causes of disease in Australia. J..E. Conner. Cray.. 59: 453–459. and R.. Smith. J. 1996..R.. M. M.. 55: 379–381. An outbreak of diarrhea and hemolytic uremic syndrome from Escherichia coli O157:H7 in fresh–pressed apple cider. Greenberg. T. Osmotic regulation of rpoS-dependent genes in Escherichia coli. Appl.M. M. Hancock. 113: 199– 207.C. Sporadic cases of hemolytic uremic syndrome associated with fecal cytotoxin and cytotoxin-producing Escherichia coli in stools.L. Kok. M. Gill. Beuchat. F.. 42: 258–263. VOL. D.W. Effect of water activity and humectant identity on the growth kinetics of Escherichia coli O157:H7. and Griffin. J. Appl.. M. M.C. C.M.T.J.B. F.O. Cray.. Escherichia coli O157:H7. D.W. Klemt.S.D. 1995. Sazie..A. Hedberg.W. and the associated hemolytic uremic syndrome. 1995.C.. Dis.L. Growth of Escherichia coli O157:H7 in modified atmosphere. Kudva. Food Protect. 48: 855– 856. Loder. 1994. 739–761. Am. 1993. Steele. Konig. Med. Raven Press Ltd. Engl. Environ.-M. 1994. Soler. Bitzan. P.. 23: 317–322. Zimmermann. Microbiol.P. R. J. Infect. Swerdlow. Guerrant.T.. T. 110: 183– 196.E. Hao. Inactivation of Escherichia coli O157:H7. J.. Microbiol. Environ. D. Expansion of response surface models for the growth of Escherichia coli O157:H7 to include sodium nitrite as a variable.. and Buchanan. L. Arocha. J. Hengge-Aronis.L. D. 1995. Food Protect. W. Experimental Escherichia coli O157:H7 carriage in calves. 1996.S. 1993. and Bagi.. K. M. 269: 883–889.J.J. N..P. Oman. and Edelson.. Ga. V. J. Buchanan.E. and Muller-Wiefel. R. 557–558. Barrett. R. Ga.L...M. M.L. L.

Lechowich. 25: 29–49... Colo. Le Saux. A. Infection caused by Escherichia coil O157:H7 in Alberta. Paton. provided that suitable credit is given. 169–213... 308: 681– 685. Doyle. Anderson. K. Raynor... 117: 812–819. I. H. Epidemiology of sporadic diarrhea due to verocytotoxin–producing Escherichia coli: A two–year prospective study.. Friesen..S. J. D.. Helgerson. 58:1307–1313. A.. Wachsmuth. D. K. 22: 269–276.C..W. N. Regulatory aspects of alkali tolerance induction in Escherichia coli. Centers for Epidemiology & Animal Health. and Rance. 1994. Bright.. Blankenhorn. 1995.P. C. K.A. Alves. Zhao. S.. P. Samadpour. Effect of trisodium phosphate on biofilm and planktonic cells of Campylobacter jejuni.. J. H. and Henning. Survival of enterohemorrhagic Escherichia coli O157:H7 during the manufacture and curing of Cheddar cheese.C. U. G.. 59: 460–464. 1995. 59: 1030–1034... Donnell. Zhao.. Riley. Gorham. 300. Karmali.. J.A. Chapin. Infect. Appl. Intern. Palumbo. and Morris. Liston. Hui. P. D. 1.S.I. Johnson.. Zhao.J.P. Blake..-L. New York. Dis. are rigorously peer-reviewed by the Expert Panel as well as by individuals outside the panel who have specific expertise in the subject.L. J. R.H.O. Wang. Dis. T. Vugia. Woodruff... K.. Dept.ift. Fort Collins. R. McNamara. Lior. Infect... IL 60601-1291 USA Tel. J. J. M. L.... McGee. J..T.T. S. J. Food Protect. Ellajosyula. Line. Moran. 42: 258–263. Am. Environ. 59: 226–229. and Doyle. Young. Johnson. and Strockbine. and Paton. Siegler. 157: 1054–1057. Taylor. Smith.. Greene. 1993. Waters.. S. K. J..C.B. L. pH and sodium nitrite. NACMCF. J. Melnychuck.A... Synergistic effect of temperature and high pH on the destruction of Salmonella enteritidis and Escherichia coli O157:H7. M.A. L.. 1995. Sutherland.L. Rice. J.. of Agriculture.L. Fate of enterohemorrhagic Escherichia coli O157:H7 in apple cider without preservatives.. S. Clarke. and Cohen. T. Food Microbiol. Wells. diagnostic and epidemiological aspects of human infection.N.L. A. Microbiol.K. 1996. R. Barrett.C. Davis. Sanhu. P. R. 1996.. Appl.J. J. An outbreak of hemolytic uremic syndrome associated with ingestion of fresh apple juice.. M. Vero cytotoxigenic Escherichia coli infection in dairy farm families.T...J. Rowbury. 60: 1038–1040.. C. J.. C. J. T. B. Microbiol. NO. Microbiol. and Williams. J. Med. N.S.. D. B. 10 . Food Protect. Escherichia coli O157:H7. IFT’s Expert Panel on Food Safety and Nutrition.. S. W. LaSalle St. B.S.H. Tilden Jr.. Y.. Schoeni.R. 58: 664–670..R. J.. 1995.B. L. M... M.M. Meyer. R. 1–2. D. H. 1987–1991. Reitsma. S. Vet.. F. H.J. Ongerth. E. The Scientific Status Summaries may be reprinted or photocopied without permission. Y.M. Predictive modeling of growth of Escherichia coli O157:H7: The effects of temperature. Infect. Sharp. Baik. Acid and base resistance in Escherichia coli and Shigella flexneri: Role of rpoS and growth pH. J. Tarr. M.M.G. S. 56: 568–572.. Jr. Rec. H. Environ. M. Reduction of Campylobacter jejuni colonization of chicks by cecumcolonizing bacteria producing anti-C. Escherichia coli O157:H7: Clinical.S. A. Appl. 1996. J. Microbiol. 34: 1622–1627..J.. 54: 762–766.G. 10: 449–488. Canada. 1993.. Rahman.I. P.L. A. Food Protect. Microbiol. B. Wilson. Appl.. J. Environ.E. Marcel Dekker. R.A. J. Microbiol.. Engl. 1996..-M. C. Food Microbiol. L. Brady. A waterborne out- The Society for Food Science and Technology 221 N. Clin. McEwen. and Marmer. Ann.D.E.. 59: 1023–1030.. J.B. J.. Inc. D. R. A. N. 61: 1290–1293. K. and Besser.L.P.D. Lett. Listeria monocytogenes and Salmonella typhimurium. D... 1995. Veterinary Services. Environ. W. Molecular characterization of Escherichia coli O157:H7 isolates form raw milk. 58: 352– 356. G.M. J. 176: 1729–1737. Lethality of heat to Escherichia coli O157:H7: D-value and z-value determinations in ground beef. Occurrence of Shiga-like toxin-producing Escherichia coli in retail fresh seafood. pp. 1992. and Dev.V. Zinser. S.S. J. Ste.. Pediatrics 91: 666–668. and Tostowaryk.. Hollingsworth. D. Generic HACCP for raw beef. D. N.G.. and Pierson. A. and D. C. Davos. 1988. 1995. Lambert-Fair. Food Microbiol. 1995.. which are not necessarily written by the Expert Panel. Microbiol. 312-782-8424 • Fax: 312-782-8348 E-mail: info@ift.. Elimination of Escherichia coli O157:H7 in meats by gamma irradiation. Martin.S. Ground beef consumption in noncommercial setting is a risk factor for sporadic Escherichia coli O157:H7 infection in Canada. Environ. Hemorrhagic colitis associated with a rare Escherichia coli serotype. Appl.. K. 1993.S C I E N T I F I C S T A T U S S U M M A R Y break in Missouri of Escherichia coli O157:H7 associated with bloody diarrhea and death. Heat resistance of Escherichia coli O157:H7 in apple juice. and in Scotland: A five-year review. Wells. P. 167: 500–502.J. and Goodson. 1996. R. Clin. Dis.. Doyle. Public Health 86: 1142–1145. Recurrent hemolytic uremic syndrome secondary to Escherichia coli O157:H7 infection. 1993. T. 22: 429–432. Lazim. J. and Besser.N... Steele.P. Griffin. Intl.A.. Med. and Brown. 1995. G. Z.J.E. Effect of heat shock and incubation atmosphere on injury and recovery of Escherichia coli O157:H7. A. Fain Jr. Gyles. 174: 1021–1027. Murrell.A. Pediatrics 101: 963–965. C. P. Microbiol. Ratcliff. 1994.. 34: 431–433. Appl. J. Dept. Escherichia coli O157:H7 shedding by feed lot cattle. Microbiol. Mechanisms of acid resistance in enterohemorrhagic Escherichia coli.A. Gastroenterology 94: 590–597. USDA/APHIS.. 1994.B. A. Tzipori. B. Microbiol. Infect.. 1992..G. J. P. D.P. National Advisory Committee on Microbiological Criteria for Foods. Jr.H. Bennett.. Med. Microbiol. Lin. N. 51.J.E. ground beef. Syemour-Murray. Verotoxigenic E. Hebert. Food Protect. M..D. McLellan.D. R. M... Welty.D. Rahn.N. 20: 333–337. Appl. M.J. Appl. and Churey.S. 1994. coli O157:H7 C O N T I N U E D chia coli O157:H7 in microbial flora of sheep. Murphy. 61: 3752–3755. J.M.A. H.. Lett.. W. Carosella.. 59: 2526–2530. Nguyen. Meng.P.W. ed.C. Custer. J.V. V. jejuni metabolites. Acid adaptation of Escherichia coli O157:H7 increases survival in acidic foods. J. 1982. Gelreich. Rowbury. Somers. W..R.E. M. Payne. M. 1994.W.. coli O157:H7 colonization of wild deer and range cattle. Food Protect. J. and poultry from grocery stores in Seattle. 1993. J.I.. Environ. D. Teo. R.. B. Lior. of Agriculture/Animal and Plant Health Service. Clin. E. Johnson.M. D. J. Lanser..L. Remis. M. Bean. 76 FOODTECHNOLOGY OCTOBER 1997 • VOL. C. E. Sims.R. and calf feces using pulsed field gel electrophoresis and plasmid DNA analysis. J. Call.. Splittstoesser. beef. Swerdlow.M. D.D. Diseases by Bacteria. Spika.. J. Infect. E. Food Protect. Tarr. 62: 3094–3100. J. Boesel. Shere. pork.B. J. Growth of Escherichia coli O157:H7 at fluctuating incubation temperatures. T. Cliver. comprises academicians representing expertise in one or more areas of food science/technology and nutrition.F... Microbiol. 1996. 1996. Werner. 137: 524. Neill. J..H. Small. 1994.org • URL: http://www. J...F. and Blake.. D.. A.. Renwick. Doyle. Bacteriol. A new route of transmission for Escherichia coli: Infection from dry fermented salami.P.A. Whittam. R. Molecular microbiological investigation of an outbreak of hemolytic-uremic syndrome caused by dry fermented sausage contaminated with Shiga-like toxin-producing Escherichia coli. J. J.. Dis.... Appl.J.M. Fate of enterohemorrhagic Escherichia coli O157:H7 in commercial mayonnaise. M. and Boyd. M.. and Johnson..J. lamb. S. In “Foodborne Disease Handbook. R.S. J. Salmonella spp.. Majkowski. Rajkowski. B. Leyer. Food Protect.D. Environ. R. and Spika.. H. N.S. which studies significant food-related issues and oversees timely production of Scientific Status Summaries. Washington. Griffin.C.. G E.J. Chicago. Johnson.. Murano.. Environ.. Pai. Woods.A. and Jackson. J.. Scientific Status Summaries. and Garber. Hancock. T.L. J.E.–L.C.A. Dis. and Trofa. Escherichia coli. Thayer. Tran. 20: 1–10. U. An assessment of environmental factors influencing acid tolerance and sensitivity in Escherichia coli. Prevalence of enterohemorrhagic Escherichia coli O157:H7 in a survey of dairy herds. J..org This and other Scientific Status Summaries are published by the Institute of Food Technologists’ Expert Panel on Food Safety and Nutrition in Food Technology. and Tarr. 19: 834–843.R. P. and Doyle. 1995.. and Foster. Intl.A.P. Schultz. Studies in gnotobiotic piglets on non–O157:H7 Escherichia coli serotypes isolated from patients with hemorrhagic colitis. and Slonczewski. 1995. T..P. 1991. T. G..M. 1983. Schoeni. Zhao.. Jr. M. Food Protect.W.. 57: 780–783. J.J. Wilson. Tippen. I.L. Bayliss...R. 1988. and Knabel.. and other enterobacteria.S. Hargrett. Appl. Minimum and maximum temperatures for growth and verotoxin production by hemorrhagic strains of Escherichia coli.R. Arbus. D. J. pp. 1993... Zhao.A.. 1995. and Braxton. Smithers. Olcott. J. and Wong.M. D. J. N..” Vol. J. R. and Doyle.. Dion.