ecoli_1097

7/22/2019 ecoli_1097

1/8FOODTECHNOLOGY 69VOL. 51, NO. 10 OCTOBER 1997

ROBERT L.BUCHANAN ANDMICHAEL P. DOYLE

he unusually virulent enterohemor-

rhagic strains ofEscher ichia coli, includ-

ing the O157:H7 serotype, have prompted foodmicrobiologists to rewrite the rule book on food

safety. These pathogens are more significant

than other well-recognized foodborne patho-

gens for reasons including the severe conse-

quences 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 destroyingenterohemorrhagic E. coli(EHEC) include cook-ing hamburgers thoroughly, incorporating a pro-cedure that kills EHEC in the manufacture of rawfermented sausage, such as salami, and pasteuriz-ing or using an equivalent processing method forapple cider. Public health problems with EHECare being recognized throughout the world. Theneed for consumer education on the safe handlingof foods has never been more acute.

Historical Perspective

E. coliO157:H7 (designated by its somatic, O,and flagellar, H, antigens) was first recognized as ahuman pathogen following two hemorrhagic coli-tis outbreaks in 1982 (Riley et al., 1983). The firstoutbreak, with 26 cases of which 19 were hospital-ized, occurred in Oregon, and the second, with 21cases and 14 hospitalizations, followed threemonths later in Michigan. Undercooked ham-burgers from the same fast food restaurant chainwere identified as the vehicle, and E. coliO157:H7was isolated from patients and a frozen groundbeef patty.

Shortly after E. coliO157:H7 was determinedto be a human pathogen, Karmali et al. (1983) ob-

served that stool samples from children with

hemolytic uremic syndrome (HUS) contained asubstance that was toxic to Vero (African greenmonkey kidney) tissue culture cells. This vero-

cytotoxin was produced by E. coliisolates, withO157:H7 the prominent serotype causing infec-tion.

Enterohemorrhagic E. coliand Foodborne Illness

E. colihas been used since 1890 as a non-pathogenic indicator of enteric pathogens, such asSalmonella. However, as knowledge of enteric dis-eases increased, investigators began isolatingstrains of E. colithat had acquired vi rulence char-acteristics causing pathogenicity to humans or an-imals. Six classes of diarrheagenic E. coliare recog-

nized: enterohemorrhagic (EHEC), enterotoxigen-ic (ETEC), enteroinvasive (EIEC), enteroaggrega-tive (EaggEC), enteropathogenic (EPEC), and dif-fusely adherent (DAEC).

Definition of EHEC.EHEC are loosely de-fined by a combination of the symptoms theyproduce and the virulence factors they possess(Neill et al., 1994). The disease-defining symptomof EHEC is hemorrhagic colitis (HC), i.e., bloodydiarrhea. Not all EHEC infections, however, pro-duce overt blood in the stools. While E. coliO157:H7 infections have a high rate of bloodystools, this may not be the case for other EHECstrains.

All EHEC strains produce Shiga toxin 1 (Stx1)and/or Shiga toxin 2 (Stx2), also referred to asverotoxin 1 (VT1) and verotoxin 2 (VT2). Theability to produce Shiga toxin was acquired from abacteriophage, presumably directly or indirectlyfrom Shigella.

The toxin is a 70,000 dalton protein composedof a single A subunit (32 kDal) and five B subunits(7.7 kDal). The B subunits provide tissue specific-ity by binding to globotriaosylceramide (Gb3) re-ceptors on the surface of eucaryotic cells. The Asubunit has an N-glycosidase that inactivates the28S ribosome, thus blocking protein synthesis.

Endothelial cells high in Gb3receptors are the pri-

T

Foodborne Disease Significance of

Escherichia coliO157:H7and Other EnterohemorrhagicE. coli

Author Buchanan, a Professional

Mem ber of IFT, is Research Mi-

crobiologist, Food Safety Re-

search Unit, U.S. Dept. of Agri-

culture, Agricultural Research

Service, 60 0 E. Mermaid Ln.,

Wyndmoor, PA 190 38 . Author

Doyle, a Professional Member of

IFT, is Director of the Center for

Food S afety and Quality En-

hanceme nt, University of Geor-

gia, Georgia Station, Griffin, GA

30223-1797 and Head of the

Dept. of Food Science and

Technology, University of Geor-

gia, Athens, GA 30 60 2.

A P U B L I C A T I O N O F

T HE I N S T I T U T E OF F OOD T E C H N OL OGI S T S

E X P E R T P A N E L O N F O O D S A F E T Y A N D N U T R I T I O N

S C I E N T I F I C S T A T U S S U M M A R Y

This Scientific

Status Summary

addresses the

virulence and

disease

characteristics of

EHEC, their

reservoirs and

sources, survival

and growth, and

disease prevention

strategies

7/22/2019 ecoli_1097

2/8

70 FOODTECHNOLOGY OCTOBER 1997 VOL. 51, NO. 10


mary target, accounting for the toxins

affinity for the colon and the renal glom-eruli, associated with HC and HUS, re-spectively. The toxin can also indirectlydamage cells by releasing cytokines, suchas tumor necrosis factor.

Toxin alone, however, is not suffi-cient to make E. colipathogenic; appar-ently nonpathogenic, stx-positive isolatesare isolated frequently from humans. Tobe fully pathogenic, EHEC require thepresence of other virulence markers. Theeaechromosomal gene, for example, isubiquitous among EHEC strains, encod-

ing for an outer membrane protein asso-ciated with attachment. Although its roleis unclear, the presence of a plasmid-en-coded enterohemolysin is characteristicof EHEC.

Disease Characteristics.Althoughthe symptoms of E. coli O157:H7 infec-tions are distinctive, they may be con-fused at any single phase with other dis-eases or conditions (Tarr, 1995; Fig. 1).The initial symptoms of HC generallyoccur 12 days after eating contaminatedfood, though longer periods (35 days)have been reported. Symptoms start withmild, nonbloody diarrhea that may befollowed by a period of crampy ab-dominal pain and short-lived fever. Theinitial diarrhea increases in intensityduring the next 2448 hr to a 4- to 10-day phase of overtly bloody diarrhea ac-companied by severe abdominal painand moderate dehydration.

Several li fe-threatening complica-tions may occur in HC patients; HUS isthe most common. The onset of HUS isapproximately a week after the onset ofgastrointestinal symptoms. Characteris-

tic symptoms are pallor, intravasculardestruction of red blood cells (microan-giopathic hemolytic anemia), depressedplatelet counts (thrombocytopenia), lackof urine formation (oligo-anuria), swell-ing (edema), and acute renal failure.HUS occurs most often in children un-der the age of 10. Approximately half ofHUS patients require dialysis, and themortality rate is 35%.

Other HUS-associated complicationsmay include seizures, coma, stroke, co-lonic perforation, pancreatitis, and hy-

pertension. Approximately 15% of cases

lead to early development of chronic

kidney failure. Insulin-dependent dia-betes may also persist in HUS patients.A small number of HUS cases may re-cur (Siegler et al., 1993).

A second complication associatedwith E. coliO157:H7 is thromboticthrombocytopenic pur-pura. This conditionresembles HUS exceptthat it generally causesless renal damage; hassignificant neurologicalinvolvement, e.g., cen-

tral nervous system de-terioration, seizures,and strokes; and is re-str icted primarily toadults (Boyce et al.,1995).

Serotypes includ-ed in EHEC.Since1982, E. coliO157:H7has been implicated inoutbreaks worldwideand is the primarycause of HC and HUSin the United States,Canada, Great Britain,and regions in Europe.The pathogen is likelyresponsible for 8595%of HUS cases (Griffin,1995). This has led toclassification of EHEClargely on the basis ofcharacteristics of sero-type O157:H7. OtherEHEC serotypes, how-ever, are reported occa-sionally in these regions, and in other

geographical areas nonO157:H7 sero-types predominate. For example, sero-types O111:H (H indicates nonmo-tile) and O157:H are more commonin Australia (Goldwater and Bettel-heim, 1995), and a high incidence ofsorbitol-positive (capable of ferment-ing sorbitol-containing culture medi-um) O157:H in central Europe hasbeen reported (Bitzan et al., 1993).Other serotypes of EHEC strains areO4:H, O11:H, O26:H11, O45:H2,O103:H2, O104:H21, O111:H8, and

O145:H (Beutin et al., 1994; Tzipori et

al., 1988).

Foods Implicated in EHEC Out-breaks. Ground beef has been the foodmost often associated with outbreaks inthe United States (Griffin and Tauxe,1991). Large outbreaks include the199293 outbreak that affected more

than 500 individuals in the western Unit-

ed States (CDC, 1993). A significant por-tion of HC infections are sporadic, i.e.,not associated with outbreaks. Groundbeef also has been implicated as a riskfactor in those sporadic infections (LeSaux et al., 1993; Pai et al., 1988).

Dry-cured salami was associatedwith an E. coliO157:H7 outbreak in thewestern United States, demonstratingthat low levels of this organism can sur-vive in acidic, fermented meats and causeillness (Tilden et al., 1996). An Austra-lian outbreak of HC and HUS resulted

from consumption of contaminated

Fig. 1 Symptoms and time courseofEscher-

ichia coliO157:H7 infection (hemorrhagic colitis)

and its primary complications (hemolytic uremic

syndrome, HUS)

E. coliO157:H7

C O N T I N U E D

7/22/2019 ecoli_1097

3/8

FOODTECHNOLOGY 71VOL. 51, NO. 10 OCTOBER 1997

O157:H7 more frequently than adults(Zhao et al., 1995).

Prevalence of fecal excretion variessubstantially among positive herds(Hancock et al., 1994; Zhao et al., 1995).

Reported incidence among cattlevaries widely, in part because of differ-ences in sensitivity of procedures used

for detecting E. coliO157:H7. Results of two major U.S. surveys

indicated that 31 (3.2%) of 965 dairycalves (Zhao et al., 1995) and 191 (1.6%)of 11,881 feedlot cattle were positive forE. coliO157:H7. An additional 0.4% offeedlot cattle were positive for E. coliO157:H (USDA/APHIS, 1995).

E. coliO157:H7 levels in calf fecesrange from

7/22/2019 ecoli_1097

4/8


of disease throughout the study. Animals

perorally administered 109E. coliO157:H7 fecally shed the bacteria for upto 92 days. A shedding sheep passed E.coliO157:H7 to a non-dosed pen mate.Diet influenced fecal shedding of E. coliO157:H7; sheep apparently negative forE. coliO157:H7 began to shed the bacte-ria when the animals were removed fromconfinement and their feed was changedfrom alfalfa pellets to sage brush andbunchgrass (Kudva et al., 1995).

Water.Drinking and recreational wa-ters have been vehicles of several out-

breaks ofE. coliO157:H7 infection(Doyle et al., 1997). A large outbreak of243 cases including four deaths was asso-ciated with contamination of municipalwater in Cabool, Mo., from December1989 to January 1990 (Swerdlow et al.,1992). Two large water mains, brokenbecause of extreme cold weather, andnew in-ground water meters may havecontributed to the outbreak. In 1991, 21cases of E. coliO157:H7 infection weretraced to swimming at a lakeside park inPortland, Ore. (Keene et al., 1994). Bath-ers, including many toddlers not yet toi-let trained, ingested fecally contaminatedlake water. Water has been suggested as avehicle of transmitting E. coliO157:H7among cattle (Faith et al., 1996).

Factors AffectingSurvival and Growth

Like all bacteria, the survival andgrowth of E. coli O157:H7 in foods aredependent on the interaction of variousintrinsic and extrinsic factors such astemperature, pH, and water activity.

Temperature.EHEC strains re-

spond to temperature in the same man-ner as non-EHEC strains, with the ex-ception of isolates of serotype O157:H7.E. coliare differentiated from other En-terobacteriaceae(family of Gram-nega-tive, catalase-positive, oxidase-negative,facultatively anaerobic rods) on the basisof their ability to grow and produce gasin EC (E. coli) broth at 44.5C. ManyO157:H7 isolates, however, do not growwell, if at all, above 44C (Doyle andSchoeni, 1984). Palumbo et al. (1995)found that the upper temperature for E.

coliO157:H7 growth was culture medi-

umdependent; all strains grew in BHI

(brain heart infusion) broth at 45C, butsix of sixteen strains did not grow in ECbroth.

The minimum growth temperaturefor E. coliO157:H7 under otherwiseoptimal conditions is approximately810C (Buchanan and Bagi, 1994; Raj-kowski and Marmer, 1995). The effect oftemperature on the growth rates of bothE. colibiotype 1 and EHEC has been de-termined, and mathematical modelshave been developed to describe howtemperature interacts with pH, water ac-

tivity, and sodium nitrite to affectgrowth kinetics (Buchanan and Bagi,1994; Gill and Phillips, 1985; Sutherlandet al., 1995).

pH.Growth rates are similar at pHvalues between 5.5 and 7.5, but declinerapidly at lower pH values (Buchananand Klawitter, 1992). The minimum pHfor E. coligrowth is 4.04.5 (Buchananand Bagi, 1994). This is dependent onthe interaction of pH with other growthparameters; for example, additionalstresses raise the minimum pH forgrowth. The type of acid (e.g., organic vsinorganic) and acid concentration influ-ence the effect of pH on E. coligrowth.Abdul-Raouf et al. (1993) reported thatin beef slurries, the relative inhibitory ac-tivity of organic acids on E. coliO157:H7was acetic > lactic citric.

When the pH falls below the mini-mum for growth, E. coliO157:H7 popu-lations decline over time. The pathogenssurvival in acidic foods is particularlyimportant, since several outbreaks havebeen associated with low levels of E. coliO157:H7 surviving in acidic foods, such

as fermented sausages, apple cider, andapple juice. The pathogen has beenshown experimentally to survive for sev-eral weeks to months in a variety of acid-ic foods, including mayonnaise (Zhaoand Doyle, 1994), sausages (Clavero andBeuchat, 1996), apple cider (Zhao et al.,1993), and Cheddar cheese (Reitsma andHenning, 1996). Survival in these foodsis extended greatly when stored at refrig-eration temperature. For example, thepathogen survived in apple cider for only23 days at 25C, compared to 1031

days at 8C (Zhao et al., 1993).

EHEC strains can have a high degree

of acid tolerance, surviving virtually un-changed during 2- to 7-hr exposures atpH 2.5 and 37C (Benjamin and Datta,1995; Buchanan and Edelson, 1996).Acid-sensitive EHEC strains, however,have also been identified. Conversely,acid-tolerant, non-enterohemorrhagicstrains have also been identified, so thisis not a characteristic unique to patho-genic isolates.

Acid tolerance in E. coliis a complexphenomenon, both growth phasede-pendent and inducible. E. colicells in the

stationary phase of growth are substan-tially more acid tolerant than cells in theexponential phase. This increased toler-ance is associated with expression ofgenes regulated by therpoSsigma factoroperon (Cheville et al., 1996; Rowbury,1995; Small et al., 1994). Lin et al. (1996)examined three mechanisms of acid re-sistance, i.e., oxidative, arginine-depen-dent, and glutamate-dependent, andfound that all three contribute to the mi-croorganisms overall acid tolerance.

Induction of acid tolerance in E. colican enhance its survival in acidic foods(Cheville et al., 1996; Leyer et al., 1995).An acid tolerant state can persist for ex-tended periods (28 days) if the cells arestored at refrigeration temperature. Theinduction of acid tolerance can also en-hance the organisms ability to surviveother stresses. Recent studies have indi-cated that induction of acid tolerancealso increases the microorganisms resis-tance to heating, radiation, and antimi-crobials (Rowbury, 1995). E. colialsopossesses an inducible alkali toleranceresponse (Rowbury et al., 1996).

Water Activity.Studies on the effectof water activity on the survival andgrowth of E. coli O157:H7 focused pr i-mari ly on the effect of sodium chloride,though, presumably,E. coli O157:H7 be-haves similarly to other E. coli. Buchananand Bagi (1994) developed a mathemati-cal model for the effects and interactionsof NaCl concentration (0.55.0%) wi thtemperature, pH, and NaNO2on thegrowth kinetics of E. coliO157:H7. Theycompared the effects of mannitol, sorbi-tol, and sucrose as humectants and con-

cluded that while humectant differences


E. coliO157:H7

C O N T I N U E D

7/22/2019 ecoli_1097

5/8


occur at limit ing aWvalues, differencesamong humectants were minimal at aW0.98 (Buchanan and Bagi, 1997). Grow-ing E. coliat elevated levels of NaCl in-duces rpoSexpression with associated in-creases in thermotolerance and H2O2re-sistance (Hengge-Aronis et al., 1993).E. coli O157:H7 can survive for many

weeks when desiccated, particularly atrefrigeration temperature (Bagi andBuchanan, 1993).

Antimicrobials.E. coli O157:H7does not appear to have any increased re-sistance to antimicrobial food additives.

Disease PreventionE. coli O157:H7 represents unique

challenges to preventing foodborne dis-ease. Its low infectious dose in combina-tion with the disease severity means thatsuccessful prevention strategies must fo-

cus on reducing or eliminating the pres-ence of the microorganism, rather thanon preventing pathogen growth, as isdone in more traditional approaches.This focus is particularly important forraw products that may not be thorough-ly cooked before consumption (e.g.,ground beef) or ready-to-eat productsthat do not receive a definitive treatmentthat assures elimination of E. coliO157:H7 (e.g., fermented sausages, applecider).

HACCP.The Hazard Analysis andCritical Control Point (HACCP) systemcontinues to be the most effective meansfor systematically developing food safetyprotocols that can reduce the risk ofEHEC infections. EHEC, however, posesome unique problems when developingand implementing HACCP plans. Forexample, the low incidence of E. coliO157:H7 in foods makes direct microbi-ological testing for the pathogen as ameans of verifying the effectiveness of aHACCP program of limited benefit. Insuch instances, verification based on mi-crobiological analysis would have to de-

pend on the use of an appropriate indi-cator organism that could provide ameasure of how well a process controlsfactors associated with risk ofE. coliO157:H7 contamination.

Most desirable is a process that in-cludes a step lethal to the pathogen. Thisreduces the critical control points to as-suring the effectiveness of that step andpreventing subsequent cross contamina-tion. For products that depend on non-thermal interventions to assure productsafety (e.g., fermented meats), validation

that the integrated process can achieve

the desired level of inactivation may be anecessary part of the hazard analysisphase of HACCP implementation.

HACCP plans that do not include astep that kills pathogens are more com-plex, since the focus is on risk reductioninstead of risk elimination. Typically,there is one or more critical control

points associated with steps that eitherreduce the likelihood that the pathogenhas gained access to the product or ac-tively reduce (but not eliminate) the lev-els that may be present.

Since such processes cannot assurecomplete absence of the pathogen, therewill also be critical control points associ-ated with preventing pathogen growth.For example, the generic HACCP planfor beef slaughter and fabrication devel-oped by the National Advisory Commit-tee on Microbiological Criteria for Foods

(NACMCF, 1993) includedE. coliO157:H7 as a hazard. The HACCP planlisted skinning, post-skinning rinsing/bactericidal spray, evisceration, final bac-tericidal rinse, chilling, and maintenanceof refrigeration as likely critical controlpoints. In addition to these specific activ-ities associated with slaughter, the com-mittee identified factors associated withanimal production practices and withthe distribution, marketing, and con-sumption of the final products thatwould have to be considered in a farm-to-table HACCP plan.

Farms.An important componentof HACCP application in animal pro-duction is reducing the carriage of E. coliO157:H7 by animals. Two approachesthat have potential are competitive ex-clusion and vaccination.

Competitive exclusion involves theuse of microbial cultures that out-com-pete pathogens from colonizing specificniches. This approach uses defined bac-terial cultures that can greatly reducecolonization of Campylobacter jejuniinpoultry (Schoeni and Doyle, 1992).

Vaccination involves exposing an an-imal to an attenuated pathogen or an an-tigen of a virulent microorganism toproduce immunity. However, traditionalvaccination approaches are not likely tobe successful with E. coliO157:H7. Re-cent observations showed that E. coliO157:H7 does not form attaching andeffacing lesions or colonize mucosal sur-faces of the gastrointestinal tract (Brownet al., 1997; Cray and Moon, 1995), andcattle exposed to E. coliO157:H7 are notprotected from reinfection (Johnson et

al., 1996). Hence, innovative approaches

will be needed for vaccines to be effec-tive.

Slaughterhouse.Like other E. coli, itis assumed that the ultimate source of E.coliO157:H7 on carcasses is fecal con-tamination during animal productionand slaughter operations. Fecal contami-nation is associated primarily with con-

tamination of the carcass during hide re-moval and spreading of contaminationto other carcasses by equipment andworkers hands (Dickson and Anderson,1992).

Traditional trimming procedures canreduceE. coli O157:H7 levels on areas ofthe carcass with visible fecal contamina-tion (Hardin et al., 1995). Various alter-natives to trimming have been investigat-ed for the removal of enteric pathogens.Recent studies with E. coliO157:H7 sug-gest that rinsing of carcass surfaces with

solutions of organic acids may have lim-ited effectiveness. Spray chil ling with 12% acetic acid only produced a 1-log cy-cle (tenfold) reduction of E. coliO157:H7 on lean tissue; a slightly greatereffect was observed on fat tissue (Dick-son, 1991). Holding the meat for 24 hrindicated only a small residual effect onlean, but a substantial effect on fat tissue.Several investigators observed differencesin the effectiveness of acid treatments be-tween lean and fat tissue and among dif-ferent portions of the carcasses (Cutterand Siragusa, 1994; Fratamico et al.,1996; Hardin et al., 1995).

Investigators found that acid rinseshad little effect on eliminating E. coliO157:H7 from the surface of beef tissues(Brackett et al., 1994; Fratamico et al.,1996), possibly due to dif ficulty in re-moving E. coliO157:H7 from beef sur-faces previously chilled (Hardin et al.,1995).

Preevisceration washing decreasedthe subsequent attachment ofE. coliO157:H7 to beef carcasses (Dickson,1995). Trisodium phosphate has been

evaluated as a sanitizing agent for carcasssurfaces and equipment. Its overall effec-tiveness, due to its high pH, was similarto that achieved with organic acids(Fratamico et al., 1996). Trisodiumphosphate can increase the removal of E.coliO157:H7 from equipment surfaces(Somers et al., 1994).

The actual fate of E. coli O157:H7cells that have been removed from car-cass surfaces by rinses with sanitizingagents is still unclear. Model systemstudies on the microorganisms ability to

survive acids and other agents at non-


7/22/2019 ecoli_1097

6/8


lethal temperatures indicate that the ex-

posure times associated with carcass san-itizing are too short to achieve any sig-nificant direct inactivation and suggestthat the primary effect is the physical re-moval of the microorganisms.

The use of steam to briefly heat car-cass surfaces to temperatures sufficientto inactivate E. coliO157:H7 while main-taining the raw character of the animaltissue is a new method for reducing thepresence of enteric pathogens on meatsand poultry. Steam vacuum systems areused for spot removal, and steam pas-

teurization cabinets are used for wholecarcass treatments. The steam vacuumsystem is reportedly capable of achievinga 5-log cycle (100,000-fold) reduction ofE. coliO157:H7 on inoculated beef sur-faces (Dorsa et al., 1996).

Food Processing.E. coliO157:H7can be controlled readily through tradi-tional thermal processing techniques;however, the organisms low infectiousdose requires that processing be suffi-cient to assure a low probability of thepathogens surviving. Dairy pasteuriza-tion processes designed to kill Coxiellaburnetti should be sufficient to eliminateE. coliO157:H7. Similarly, pasteurizationwould be expected to controlE. coliO157:H7 in fruit juices.

D-values (decimal reduction time, orthe time required to destroy 90% of thepopulation) have been determined at anumber of different temperatures in var-ious ground meat and poultry products(Ahmed et al., 1995; Doyle and Schoeni,1984; Line et al., 1991). For example, re-ported D60Cvalues for serotype O157:H7in ground products range from 0.4 to 0.8

min.D-values vary to some degree among

ground products; however, thermal resis-tance is more strongly influenced by fatcontent, i.e., the higher the fat content,the greater the thermal resistance.Splittstoesser et al. (1995) estimated thatthe D60Cfor E. coliO157:H7 in applejuice (pH 4.0) was 0.4 min. Prior heatshock increases thermal resistance, andanaerobic incubation increases recoveryof heated cells (Murano and Pierson,1993). Cells held at refrigeration are

more sensitive than cells heated directly

from the frozen state (Jackson et al.,1995). Elevated pH values (pH 1011)can enhance the thermal destruction ofE. coliO157:H7 (Teo et al., 1996).

Outbreaks associated wi th raw milkhave prompted investigations into thefate of E. coliO157:H7 in dairy products.The pathogen persisted during the man-ufacture of cottage cheese (Arocha et al.,1992) and Cheddar cheese (Reitsma andHenning, 1996) made from inoculatedmilk. The organism is inactivated readily

by pasteurization of milk, and levels de-clined during aging of the Cheddarcheese.

Alternative technologies to thermalprocessing that could eliminate or con-trol E. coliO157:H7 while maintainingthe raw character of foods are currentlybeing investigated. One that has poten-tial, particularly for meat and poultryproducts, is ionizing radiation. Thepathogen is relatively radiation sensitive,and radiation pasteurization doses of1.53.0 kGy appear to be sufficient to

eliminate it at the levels that they are

likely to occur at in ground beef (Clavero

et al., 1994; Thayer and Boyd, 1993). Ra-diation inactivation is temperature de-pendent; higher doses are required whenground beef is irradiated at frozen tem-peratures. There appears to be little dataon the abili ty of ir radiation to control E.coliO157:H7 on fruits and vegetables,though recent studies (Buchanan et al.,unpublished data) indicate that low-doseirradiation of apple cider is effective.

While food processing research withE. coliO157:H7 has concentrated onproducts of animal origin, an increasing

number of outbreaks have involvedfruits and vegetables. E. coli O157:H7strains have been shown to grow onmany vegetables if stored at tempera-tures that support growth (Abdul-Raoufet al., 1993). Modified-atmosphere pack-aging, used extensively with produce,does not prevent the growth ofE. coliO157:H7 (Abdul-Raouf et al., 1993; Haoand Brackett, 1993).

Home and Foodservice.Food han-dling and preparation practices can con-tr ibute to E. coliO157:H7 infections andconversely play an important part intheir prevention. Undercooking has beenan important contributing factor in E.coliO157:H7 outbreaks associated withground beef. Adherence to good foodhandling practices recommended forfoodservice and home preparation rep-resent the last line of defense for assuringprevention ofE. coli O157:H7 infection(Table 2). Infected food handlers couldpotentially serve as foci forE. coliO157:H7 infections, particularly duringthe first 48 hr of an infection whensymptoms are sti ll relatively mi ld or in

those individuals who do not have overt-ly bloody stools. In particular, adequatecooking temperatures and times, preven-tion of cross contamination between rawand cooked foods, and appropriate re-frigerated storage are key factors for re-ducing the risks associated with E. coliO157:H7.

SummaryIt is apparent that microbiologists,

molecular biologists, and food scientistshave made great strides in understanding

E. coliO157:H7 and related EHEC and


Table 2 Recommendationsto reduce the risk of acquir-ing an Escherichia coliO157:H7 infection

1. Cook ground beef and venisonthoroughly (minimum 160F) beforeeating.

2. Drink only pasteurized milk and applejuice.

3. Wash fresh fruits and vegetablesthoroughly before eating.

4. Wash hands thoroughly after handlinganimals, particularly cattle, deer, goats,

or dogs.

5. Wash hands thoroughly after changingdiapers or after providing care to childrenor adults suffering from a diarrhealdisease.

6. Do not use fresh manure fromruminants to fertilize vegetables or fruits.

7. Avoid swimming in lakes or pondsused by cattle and drinking surfacewater that has not been properly treatedto eliminate pathogens.

E. coliO157:H7

C O N T I N U E D

7/22/2019 ecoli_1097

7/8


developing means for controlling themin foods. It is also evident, however, thatthere are major scientific questions thatmust be answered before we will be ableto fully assess and manage public healthconcerns associated with their food-borne transmission. Addressing thesequestions will require the continued ef-

fort and support of basic and appliedscientists from a variety of disciplines.

On a broader front, a key lesson dra-matically reinforced by the emergence ofE. coli O157:H7 is that both the macro-scopic and microscopic worlds changecontinually. We cannot take for grantedthat foods and food practices that havebeen traditionally safe will remain thatway in the future. Continued vigilanceand the ability to rapidly mobilize re-search capabilities must be an integralpart of food safety programs if we are

going to minimize the impact of newfoodborne microbial threats to humanhealth.

ReferencesAbdul-Raouf, U.M., Beuchat, L.R., and Am mar, M.S.

1993. Survival and growth of Escherichia coliO15 7: H7 on salad vegetables. Appl. Environ. Microbi-o l. 5 9 : 1 9 9 9 2 0 0 6 .

Ahmed, N.M ., Conner, D.E., and Huffman, D.L. 19 95 .Heat-resistance of Escherichia coli O157:H7 in meatand poultry as affected by product co mposition. J.Food Sc i. 60 : 606 61 0 .

Arocha, M.M ., M cVey, M. , Loder, S.D., Rupnow, J.H.,and Bullerman, L. 1992. Behavior of hemorrhagicEscherichia coli O157:H7 during the manufacture ofcottage cheese. J. Food Protect. 55 : 37 9 38 1.

Bagi, L.K. and Buchanan, R.L. 1993. Preservation ofListeria mo nocytogenes and other pathogenic food-borne bacteria on silica gel. Lett. Appl. Microbiol. 17 :3 7 3 9 .

Belongia, E.A., Osterholm, M.T., Soler, J.T., Ammend,D.A., Braun, J.E., and MacD onald, K.L. 19 93 . Trans-mission of Escherichia coli O157:H7 infection in Min-nesota child day-care facilities. J. Am. Med. Assn. 2 69 :8 8 3 8 8 9 .

Benjamin, M.M. and Datta, A.R. 1995. Acid tolerance ofenterohemorrhagic Escherichia coli. Appl. Environ. Mi-crob io l . 61 : 16691672 .

Besser, R.E., Lett, S.M., Weber, J.T., Doyle, M.P., Barrett,T.J., Wells, J.G., and Griffin, P.M. 1993. An outbreak ofdiarrhea and hemolytic uremic syndrome from Escheri-

chia coliO157:H7 in freshpressed apple cider. J. Am.Med . Assn . 269 : 2217 22 20 .

Beutin, L., Aleksic, S., Zimmermann, S., and Gleier, K.19 94 . Virulence factors and phenotypical traits of vero-toxigenic strains of Escherichia coli isolated from hu-man patients in Germany. Med . M icrobiol. Imm unol.1 8 3 : 1 3 2 1 .

Bitzan, M. , Lidwig, K., Klemt, M., Konig, H., Buren, J.,and Muller-W iefel, D.E. 19 93 . The role of Escherichiacoli infections in the classical (enteropathogenic)hemolytic uraemic syndrome: Results of a central Euro-pean, multicenter study. Epidemiol. Infect. 110: 1831 9 6 .

Boyce, T.G., Swerdlow, D.L., and Griffin, P.M. 1995. Es-cherichia coli O157:H7 and the hemolytic uremic syn-drome. N. Engl. J. Med. 333 : 364 3 68 .

Brackett, R.E., Hao, Y.-Y., and Doyle, M .P. 1 99 4. Ineffec-

tiveness of hot acid sprays to decontaminate Escheri-chia coli O157 :H7 on beef. J. Food Protect. 57: 19 82 0 3 .

Brown, C.A., Harmon, B.G., Zhao, T., and Doyle, M.P.1997. Experimental Escherichia coliO15 7:H7 carriagein calves. Appl. Environ. Microbiol. 63: 2732.

Buchanan, R.L. and Bagi, L.K. 1994. Expansion of re-sponse surface models for the growth of EscherichiacoliO15 7: H7 to include sodium nitr ite as a variable.Int l . J. Food Microbio l . 23: 31 7 32 2.

Buchanan, R.L. and Bagi, L.K. 1997. Effect of water ac-tivity and hum ectant identity on the growth k inetics ofEscherichia coliO157:H7. Food Microbiol. (In press).

Buchanan, R.L. and Edelson, S.G. 1 99 6. Culturing en-terohemorrhagic Escherichia coli in the presence andabsence of glucose as a simple m eans of evaluatingthe acid tolerance of stationary-phase cells. Appl. Envi-ron. M icrob io l . 62 : 400 9 401 3 .

Buchanan, R.L. and Klawitter, L.A. 1 99 2. The effect ofincubation temperature, initial pH, and sodium chlorideon the growth kinetics of Escherichia coli O157 :H7 .Food Microbio l . 9 : 185196.

CDC. 199 3. Upd ate: Multistate outbreak of EscherichiacoliO15 7:H7 in fect ions from hamburgers westernUnited States, 19921993. Centers for Disease Con-trol and Prevention, Atlanta, Ga., Morb. Mortal. Weekly

Rep t . 42 : 258263 .CDC. 1995. Community outbreak of hemolytic uremic

syndrome attr ibutable to Escherichia coli O111 :NMSouth Australia. Centers for Disease Control and Pre-vention, Atlanta, Ga., M orb. Mortal. Weekly Rept. 44 :5 5 0 5 5 1 , 5 5 7 5 5 8 .

Cheville, A.M., Arnold, K.W., Buchrieser, C., Cheng, C.-M.,and Kaspar, C.W. 19 96 . rpoS regulation of acid, heat,and salt tolerance in Escherichia coliO157:H7. Appl.Environ. Microbio l . 62: 18221824.

Clavero, M.R.S. and Beuchat, L.R. 19 96 . Survival of Es-cherichia coli O157:H7 in broth and processed salamias influenced by pH, water activity, and temperatureand suitability of media for its recovery. Appl. Environ.Microb io l. 62 : 27 35 274 0 .

Clavero, M.R.S., Mo nk, J.D., Beuchat, L.R., Doyle, M. P.,

and Brackett, R.E. 1994. Inactivation of EscherichiacoliO157:H7, salmonellae, and Campylobacter jejuniin raw ground beef by gamma irradiation. Appl. Envi-ron. M icrob io l . 60 : 206 9 207 5 .

Cray, W.C. and Moon, H.W. 1 99 5. Experimental infectionof calves and adult cattle with Escherichia coliO157:H7. Appl. Environ. Microbio l . 61: 15861590.

Cutter, C.N. and Siragusa, G.R. 1994. Efficacy of organicacids against Escherichia coliO157 :H7 attached tobeef carcass tissue using a pilot scale model carcasswasher. J. Food Protect. 57: 97103.

Dickson, J.S. 1991. Control of Salmonella typhimurium,Listeria m onocytogenes, and Escherichia coliO157 :H7on beef in a m odel spray chilling system. J. Food Sci.5 6 : 1 9 1 1 9 3 .

Dickson, J.S. 19 95 . Susceptibility of preeviscerationwashed beef carcasses to c ontamination by Escheri-chia coli O157:H7 and salmonellae. J. Food Protect.5 8 : 1 0 6 5 1 0 6 8 .

Dickson, J.S. and Anderson, M.E. 1992. Microbiologicaldecontamination of food animal carcasses by w ashingand sanitizing systems: A review. J. Food Protect. 55:1 3 3 1 4 0 .

Dorsa, W.J., Cutter, C.N., and Siragusa, G.R. 1996. Effec-tiveness of a steam vacuum sanitizer for reducing Es-cherichia coliO157:H7 inoculated to beef carcass sur-face tissue. Lett. Appl. Microbiol. 23: 6163.

Doyle, M. P. and Schoeni, J.L. 19 84 . Survival and growthcharacteristics of Escherichia coliassociated with hem-orrhagic co litis. Appl. Environ. Microbiol. 48 : 85 58 5 6 .

Doyle, M .P., Zhao, T., M eng, J., and Zhao, S. 19 97 . Es-cherichia coliO157:H7. In Food Microbiology: Funda-

mentals and Frontiers, ed. M.P. Doyle, L.R. Beuchat,

and T.J. Montville, pp. 17 1 19 1. ASM Press, Washing-ton, D.C.

Faith, N.G., Shere, J.A., Brosch, R., Arnold, K.W., Ansay,S.E., Lee, M.-S., Luchansky, J.B., and Kaspar, C.W.1996. Prevalence and clonal nature of Escherichia coliO157:H7 on dairy farms in Wisconsin. Appl. Environ.Microb io l . 62 : 15191525 .

Fratamico, P.M., Buchanan, R.L., and Cooke, P.H. 1 99 3.Virulence of an Escherichia coliO15 7:H7 sorb ito l-posi-t ive m utant. Appl. Environ. Microbio l . 59: 42 45 4 25 2.

Fratamico, P.M., Schultz, F.J., Benedict, R.C., Buchanan,R.L., and Cook e, P.H. 1 99 6. Factors influencing at-tachment of Escherichia coli O157:H7 to beef tissuesand removal using selected sanitizing rinses. J. FoodPro tect . 59 : 453 459 .

Gill, C.O. and Phillips, D.M. 1985. The effect of mediacom position on the relationship between tem peratureand growth rate of Escherichia coli. Food Microbiol. 2:2 8 5 2 9 0 .

Goldwater, P.N. and Bettelheim, K.A. 19 95 . The role ofenterohemorrhagic Escherichia coliserotypes otherthan O15 7:H 7 as c auses of disease in Australia. Com-mun. Dis. Intell. 19: 24.

Griffin, P.M. 1 99 5. Escherichia coliO157 :H7 and otherenterohemorrhagic Escherichia coli. In Infections ofthe Gastrointestinal Tract, ed. M.J. Blaser, P.D. Smith,

J.I. Ravdin, H.B. Greenberg, and R.L. Guerrant, pp.73 9 76 1. Raven Press Ltd., New York.

Griffin, P.M. and Tauxe, R.V. 1991. The epidemiology ofinfections caused by Escherichia coli O157:H7, otherenterohemorrhagic E. coli, and the associated hemolyt-ic uremic syndrome. Epidemiol. Rev. 13: 6098.

Hanco ck, D.D., Besser, T.E., Kinsel, M. L., Tarr, P.I., R ice,D.H., and Paros, M.G. 19 94 . The prevalence of Es-cherichia coliO157:H7 in dairy and beef cattle inWashington state. Epidemiol. Infect. Dis. 113 : 19 92 0 7 .

Hao, Y.Y. and Brackett, R.E. 1993. Growth of EscherichiacoliO157:H7 in modified atmosphere. J. Food Protect.5 6 : 3 3 0 3 3 2 .

Hardin, M.D., Acuff, G.R., Lucia, L.M ., Om an, J.S., andSavell, J.W. 1995. Comparison of methods for decon-

tamination from beef carcass surfaces. J. Food Protect.5 8 : 3 6 8 3 7 4 .Hengge-Aronis, R., Lange, R., Henneberg, N., and Fis-

cher, D. 199 3. Osm otic regulation of rpoS-dependentgenes in Escherichia coli. J. Bacter io l . 175: 259265.

Jackson, T.C., Hardin, M.D., and Acuff, G.R. 1 99 5. Heatresistance of Escherichia coliO157:H7 in a nutrientmedium and in ground beef patties as influenced bystorage and holding temperatures. J. Food Protect. 59 :2 3 0 2 3 7 .

Johnson, R.P., Cray, Jr., W.C., and Johnson, S.T. 1996.Serum antibody responses of cattle following experi-mental infection with Escherichia coliO157 :H7. In fect.Im m u n. 6 4 : 1 8 7 9 1 8 8 3 .

Karmali, M.A., Steele, B.T., Petric, M. , and Lim, C. 1 98 3.Sporadic cases of hemolytic uremic syndrome associ-ated with fecal cytotoxin and cytotoxin-producing Es-cherichia coliin stools. Lancet i: 61 9 62 0.

Keene, W.E., McAnulty, J.M., Hoesley, F.C., Williams, L.P.,Hedberg, K., Oxman, G.L., Barrett, T.J., Pfaller, M.A.,and Fleming, D.W. 1994. A swimming-associated out-break of hem orrhagic c olitis caused by Escherichia coliO157 :H7 and Shigella sonnei. N. Engl. J. Med.3 3 1 : 5 7 9 5 8 4 .

Keene, W.E., Sazie, E., Kok, J., Rice, D.H., Hancock,D.D., Balan, V.K., Zhao, T., and Doyle, M.P. 1997. Out-break of Escherichia coli O157:H7 infections traced tojerk y m ade fro m de er m eat . J. A m . M ed . A ssn . 2 7 7 :1 2 2 9 1 2 3 1 .

Kudva, I.T., Hatfield, P.G., and Hovde, C.J. 1995. Effect ofdiet on the shedding of Escherichia coli O157:H7 in asheep model. Appl. Environ. Microbiol. 61: 13631 3 7 0 .

Kudva, I.T., Hatfield, P.G., and Hovde, C.J. 1996. Escheri-


7/22/2019 ecoli_1097

8/8


chia coliO15 7:H 7 in m icrobial flora of sheep. Appl.

Environ. Microbio l. 34 : 43 1 43 3.Le Saux, N., Spika, J.S., Friesen, B., Johnson, I., Melny-

chuck, D., Anderson, C., Dion, R., Rahman, M. , andTostowaryk, W. 1993. Ground beef consumption innoncomm ercial setting is a risk factor for sporadic Es-cherichia coliO15 7:H 7 infection in Canada. J. Infect.D is . 167 : 500502 .

Leyer, G.J., Wang, L.-L., and Johnson, E.A. 1995. Acidadaptation of Escherichia coliO157:H7 increases sur-vival in acidic foods. Appl. Environ. Microbiol. 61:3 7 5 2 3 7 5 5 .

Lin, J., Smith, M.P., Chapin, K.C., Baik, H.S., Bennett,G.N., and Foster, J.W. 19 96 . Mec hanisms of acid re-sistance in enterohemorrhagic Escherichia coli. Appl.Environ. Microbio l . 62: 30943100.

Line, J.E., Fain Jr., A.R., Moran, A.B., Martin, L.M.,

Lechowich, R.V., Carosella, J.M. , and Brown, W.L.1991. Lethality of heat to Escherichia coli O157 :H7 :D-value and z-value determinations in ground beef. J.Food Protect. 54: 762766.

Meng, J., Zhao, S., Zhao, T., and Doyle, M.P. 19 95 . Mo-lecular characterization of Escherichia coliO157 :H7isolates form raw milk, ground beef, and calf feces us-ing pulsed field gel electrophoresis and plasmid DNAanalysis. J. Med. Microbiol. 42: 258263.

Murano, E.A. and Pierson, M.D. 19 93 . Effect of heatshock and incubation atmosphere on injury and recov-ery of Escherichia coliO15 7:H7. J. Food Protect. 56:5 6 8 5 7 2 .

NACMCF. 1 99 3. Generic HACCP for raw beef. NationalAdvisory Comm ittee on M icrobiological Criteria forFoods, U.S. Dept. of Agriculture. Food Microbiol. 10:4 4 9 4 8 8 .

Neill, M.A., Tarr, P.I., Taylor, D.N., and Trofa, A.F. 1994.Escherichia coli. In Foodborne Disease Handbook,Diseases by Bacteria, Vol. 1, ed. Y.H. Hui, J.R.Gorham, K.D. Murrell, and D.O. Cliver, pp. 16 9 21 3.Marcel Dekker, Inc., New York.

Pai, C.H., Lior, A.N., Johnson, W.M., Sims, H.V., Woods,D.E. 19 88 . Epidemiology of sporadic diarrhea due toverocytotoxinproducing Escherichia coli: A twoyear

prospective study. J. Infect. Dis. 157: 10541057.Palumbo, S.A., Call, J.E., Schultz, F.J., and Williams, A.C.

19 95 . M in imum and maximum temperatures forgrowth and verotoxin production by hem orrhagicstrains of Escherichia coli. J. Food Protect. 58: 3523 5 6 .

Paton, A.W., Ratcliff, R.M., Doyle, R.M., Syemour-Murray,J., Davos, D., Lanser, J.A., and Paton, J.C. 19 96 . Mo -

lecular microbiological investigation of an outbreak ofhemolytic-uremic syndrome caused by dry fermentedsausage contaminated with Shiga-like toxin-producingEscherichia coli. J. Cl in . Microbio l. 34: 1 62 2 16 27 .

Rajkowski, K.T. and M armer, B.S. 199 5. Growth of Es-cherichia coliO157:H7 at fluctuating incubation tem-peratures. J. Food Protect. 58:1 30 7 13 13 .

Reitsma, C.J. and Henning, D.R. 1 99 6. Survival of en-terohemorrhagic Escherichia coliO157 :H7 dur ing themanufacture and curing of Cheddar cheese. J. FoodPro tect . 59 : 460 46 4 .

Rice, D.H., Hancock, D.D., and Besser, T.E. 1995. Vero-toxigenic E. coliO157:H7 colonization of wild deer andrange cattle. Vet. Rec. 137: 524.

Riley, L.W., Remis, R.S., Helgerson, S.D., McGee, H.B.,Wells, J.G., Davis, B.R., Hebert, R.J., Olcott, H.M.,

Johnson, L.M., Hargrett, N.T., Blake, P.A., and Cohen,

M.L. 1983. Hemorrhagic colitis associated with a rareEscherichia coliserotype. N. Engl. J. Med. 308: 6816 8 5 .

Rowbury, R.J. 1 99 5. An assessment of environmentalfactors influencing acid tolerance and sensitivity in Es-cherichia coli, Salmonellaspp. and other enterobacte-r ia . Lett. Appl. Microbio l . 20: 3 33 3 37 .

Rowbury, R.J., Lazim, Z., and Goodson, M. 1996. Regu-latory aspects of alkali tolerance induction in Escheri-chia coli. Lett. Appl. Microbio l . 22: 42 9 43 2.

Samadpour, M., Ongerth, J.E., Liston, J., Tran, N., Nguy-en, D., Whittam, T.S., Wilson, R.A., and Tarr, P.I. 1994.Occurrence of Shiga-like toxin-producing Escherichiacoli in retail fresh seafood, beef, lamb, pork, and poultryfrom grocery stores in Seattle, Washington. Appl. Envi-ron. M icrob io l . 60 : 103 8 104 0 .

Schoeni, J.L. and Doyle, M.P. 1992. Reduction ofCampylobacter jejunicolonization of chicks by cecum-colonizing bacteria producing anti-C. jejuni metabolites.Appl. Environ. Microbio l. 58 : 66 4 67 0.

Siegler, R.L., Griffin, P.M., Barrett, T.J., and Strockbine,N.A. 1993. Recurrent hemolytic uremic syndrome sec-ondary to Escherichia coli O157:H7 infection. Pediat-r i cs 91 : 666668 .

Small, P., Blankenhorn, D., Welty, D., Zinser, E., and Slon-czewski, J.L. 1994. Acid and base resistance in Es-

cherichia coliand Shigella flexneri: Role of rpoSa ndgrowth pH. J. Bacter io l . 176: 17291737.

Somers, E.B., Schoeni, J.L., and Wong, A.C.L. 1 99 4. Ef-fect of tr isodium phosphate on b iofilm and planktoniccells of Campylobacter jejuni, Escherichia coliO157 :H7 , Listeria m onocytogenesand Salmonella ty-phimurium. In tl . J. Food Microbio l . 22: 2 69 2 76 .

Splittstoesser, D.F., McLellan, M.R., and Churey, J.J.1995. Heat resistance of Escherichia coliO157 :H7 inapple juice. J. Food Protect. 59: 226229.

Steele, B.T., Murp hy, N., Arbus, G.S., and Rance, C.P.1982. An outbreak of hemolytic uremic syndrome as-sociated with ingestion of fresh apple juice. J. Pediatrics1 0 1 : 9 6 3 9 6 5 .

Sutherland, J.P., Bayliss, A.J., and Braxton, D.S. 1995.Predictive mo deling of growth of Escherichia coli

O157:H7: The effects of temperature, pH and sodiumnitr ite. Intl. J. Food Microbiol. 25: 2949.Swerdlow, D.L., Woodruff, B.A., Brady, R.C., Griffin, P.M.,

Tippen, S., Donnell, H.D. Jr., Gelreich, H.D., Payne,B.J., Meyer, A. Jr., Wells, J.G., Greene, K.D., Bright, M.,Bean, N.H., and Blake, P.A. 1 99 2. A w aterborne out-

break in M issouri of Escherichia coliO157 :H7 associ-ated with bloody d iarrhea and death. Ann. Intern. M ed.1 1 7 : 8 1 2 8 1 9 .

Tarr, P.I. 1995. Escherichia coliO157:H7: Clinical, diag-nostic and epidemiological aspects of human infection.Clin. Infect. Dis. 20: 110.

Teo, Y.L., Raynor, T.J., Ellajosyula, K.R., and Knabel, S.J.1996. Synergistic effect of temperature and high pHon the destruction of Salmonella enteritidisand Escher-ichia coli O157:H7. J. Food Protect. 59: 10231030.

Thayer, D.W. and Boyd, G. 1993. Elimination of Escheri-chia coliO157:H7 in meats by gamma irradiation.Appl. Environ. Microbio l. 59 : 10 30 1 03 4.

Tilden Jr., J., Young, W., McNamara, A.-M., Custer, C.,Boesel, B., Lamb ert-Fair, M .A., Majkowski, J., Vugia,D., Werner, S.B., Hollingsworth, J., and Morris, J.G. Jr,J.G. 19 96 . A new route of transmission for Escherichiacoli: Infection from dry fermented salami. Am. J. PublicHea l th 86 : 11421145 .

Tzipori, S., Wachsmuth, I.K, Smithers, J., and Jackson, C.19 88 . Studies in gnotobiotic p ig lets on nonO15 7:H7Escherichia coli serotypes isolated from patients withhemorrhagic colitis. Gastroenterology 94: 590597.

USDA/APHIS. 19 95 . Escherichia coliO157:H7 sheddingby feed lot cattle. pp. 1 2. Centers for Epidemiology &Animal Health, Veterinary Services, U.S. Dept. of Agri-

culture/Animal and Plant Health Service, Fort Collins,Colo.

Waters, J.R., Sharp, J.C.M., and Dev, V.J. 1994. Infectioncaused by Escherichia coilO157:H7 in Alberta, Cana-da, and in Scotland: A five-year review, 19871991.Cl in . Infect. Dis. 19: 8 34 8 43 .

Wilson, J.B., Clarke, R.C., Renwick, S.A., Rahn, K.,Johnson, R.P., Karmali, M.A., Lior, H., Alves, D., Gyles,C.L., Sanhu, K.S., McEwen, S.A., and Spika, J.S.1996. Vero cytotoxigenic Escherichia coli infection indairy farm families. J. Infect. Dis. 174: 10211027.

Zhao, T. and Do yle, M .P. 1 99 4. Fate of enterohemorrhag-ic Escherichia coliO15 7:H7 in commercial mayon-naise. J. Food Protect. 57: 78 0 78 3.

Zhao, T., Doyle, M.P., and Besser, R.E. 1993. Fate of en-terohemorrhagic Escherichia coliO157 :H7 in apple ci-

der w ithout preservatives. Appl. Environ. Microbiol. 5 9:2 5 2 6 2 5 3 0 .Zhao, T., Doyle, M.P., Shere, J., and Garber, L. 1995.

Prevalence of enterohemorrhagic Escherichia coliO15 7: H7 in a survey of dairy herds. Appl. Environ. Mi-crob io l . 61 : 12901293 .


The Society for Food Science and Technology

221 N. LaSalle St., Ste. 300, Chicago, IL 60601-1291 USA

Tel. 312-782-8424 Fax: 312-782-8348

E-mail: [email protected] URL: http://www.ift.org

This and other Scientific Status Summaries are published by the Institute of Food Technologists

Expert Panel on Food Safety and Nutrition inFood Technology. Scientific Status Summaries, which

are not necessarily written by the Expert Panel, are rigorously peer-reviewed by the Expert Panel

as well as by individuals outside the panel who have specific expertise in the subject. IFTs Expert

Panel on Food Safety and Nutrition, which studies significant food-related issues and oversees

timely production of Scientific Status Summaries, comprises academicians representing exper-

tise in one or more areas of food science/technology and nutrition.

The Scientific Status Summaries may be reprinted or photocopied without permission, provided

that suitable credit is given.

E. coliO157:H7

C O N T I N U E D

ecoli_1097

Documents