Escherichia coli Serotype O157:H7: 

Novel Vehicles of Infection and 

Emergence of Phenotypic Variants

Peter Feng, Ph.D.

U.S. Food and Drug Administration, Washington, D.C., USA

Escherichia coli serotype O157:H7 was only recognized as a human pathogen a

little more than a decade ago, yet it has become a major foodborne pathogen. In the

United States, the severity of serotype O157:H7 infections in the young and the elderly

has had a tremendous impact on human health, the food industry, and federal

regulations regarding food safety. The implication of acidic foods as vehicles of

infection has dispelled the concept that low-pH foods are safe. Further, the association

of nonbovine products with outbreaks suggests that other vehicles of transmission

may exist for this pathogen. In laboratory diagnosis, most microbiologic assays rely

on a single phenotype to selectively isolate this pathogen. However, the increasing

evidence that phenotypic variations exist among isolates in this serogroup may

eventually necessitate modifications in assay procedures to detect them.

Enterohemorrhagic Escherichia coli (EHEC) has

emerged in recent years as the predominant cause

of hemorrhagic colitis in humans. This illness, with

characteristic symptoms of bloody diarrhea and abdominal cramps, can progress into a more severe,

life-threatening complication known as hemolytic

uremic syndrome (HUS). The pathogenicity of

EHEC appears to be associated with a number of

virulence factors, including the production of several

cytotoxins (1,2). These toxins are collectively referred to as verotoxins or Shiga-like toxins (SLTs)

because the SLT-I of E. coli closely resembles the

Shiga toxin of Shigella dysenteriae type 1 (2). Although more than 60 E. coli serotypes produce SLTs

(2) and more are being identified as capable of producing SLT, serotype O157:H7 is the predominant

pathogen in the EHEC group and the one associated

most frequently with human infections worldwide.

Isolates of the serotype O157:H7 were first implicated in foodborne illness in 1982; in the subsequent

10 years, approximately 30 outbreaks were recorded

in the United States (1). In early 1993, however,

serotype O157:H7 received considerable attention

after a large foodborne disease outbreak, traced to

the consumption of undercooked, contaminated

hamburgers served at a regional fast-food restaurant (3). More than 700 persons in four states were

infected; there were 51 cases of HUS and four

deaths. Since that outbreak, the reported incidence

of serotype O157:H7 infections has risen, partly

because better surveillance systems have been implemented and awareness has increased among physicians, clinical microbiologists, and consumers.

Fifteen additional outbreaks were recorded in 1993

and 20 in the first half of 1994.

Because serotype O157:H7 has only recently been

recognized as a foodborne pathogen, our knowledge

is limited. However, the notoriety of recent outbreaks and the severity of serotype O157:H7 infections have stimulated research on the organism, its

ecology, antibiotic resistance properties, and virulence factors. Much has already been learned from

the epidemiologic investigations of past outbreaks.

For instance, foodborne infections of serotype

O157:H7 have most often been associated with the

consumption of bovine products; however, several

recent outbreaks have implicated other less likely

vehicles of infection and showed that the organism

may have some unsuspected characteristics. Although genotypic studies show serotype O157:H7 to

be a unique clone only distantly related to other E.

coli serotypes (4,5), phenotypic diversity within the

serogroup (6) may complicate existing laboratory

diagnosis procedures. The introduction of various

molecular diagnostic techniques may facilitate the

detection of this serotype and its phenotypic variants.

This review examines unexpected and seemingly

unlikely vehicles implicated in recent serotype

O157:H7 outbreaks and the impact of emerging phenotypic variants and their effect on diagnostic assays used to detect this pathogen in clinical

specimens or in the food supply.

Novel Vehicles of Transmission

So far, serotype O157:H7 has caused a total of 60

outbreaks of foodborne illness in the United States.

Consumption of contaminated, undercooked

Address for correspondence: Peter Feng (HFS-516), 

U.S. Food and Drug Administration, 200 C Street, S.W.,

Washington, DC 20204, USA; fax 202-401-7740; 

e-mail pxf@fdacf.ssw.dhhs.gov.

Synopsis

Vol. 1, No. 2 — April-June 1995 47 Emerging Infectious Diseases
ground-beef products has accounted for most outbreaks; however, raw milk was also implicated in

several outbreaks in the United States and Canada.

Improper hygiene with secondary spread from person-to-person contact is another well-documented

route of infection (1,2). In the last few years, however, several foodborne outbreaks of serotype

O157:H7 have implicated unique and seemingly unlikely vehicles of infection: among them are acidic

foods, fruits, salad vegetables, yogurt, and water.

Acidic foods

In the Retail Food Store Sanitation Code of the

U.S. Food and Drug Administration, foods with a pH

value of less than 4.6 are generally regarded as low

risk in terms of food safety. However, several recent

disease outbreaks attributable to serotype O157:H7

have shown that this pathogen can persist in foods

with low pH.

In the fall of 1991, an outbreak of serotype

O157:H7 that affected 23 persons was traced to the

consumption of fresh-pressed apple cider (7). The

implicated cider, made from unwashed “dropped”

apples at a farm, had a pH value of 3.7 to 3.9, was

not pasteurized, and contained no preservatives.

Although apple cider had been implicated in a previous outbreak of Salmonella typhimurium, it is not

a common vehicle of enteric infection because of its

high acidity. Several laboratory studies have subsequently demonstrated that isolates of serotype

O157:H7 can tolerate acidic conditions. Some

strains persist in media with pH values as low as 2.0

(8), and in cold (8°C) apple cider for 10 to 31 days

(7,9). Although the source of serotype O157:H7 in the

cider that caused illness was never fully established,

it was suspected that the dropped apples had been

contaminated by cow manure. 

The ability of serotype O157:H7 to tolerate acidity

was substantiated in 1993, when another acidic food

was implicated in a series of restaurant outbreaks

that infected at least 48 persons. Although the

source of the outbreaks was not conclusively identified, epidemiologic investigations and other data

implicated mayonnaise or mayonnaise-based dressing and sauces. Samples of mayonnaise had a pH of

3.6 to 3.9, and the sauces prepared from it were also

acidic, with pH levels of 3.6 to 4.4 (10). After this

outbreak, several studies confirmed that although

isolates of serotype O157:H7 do not multiply under

these conditions, they can persist in commercial

mayonnaise up to 55 days at 5°C (10,11). How the

mayonnaise became contaminated with serotype

O157:H7 was not determined; however, improper

handling of bulk mayonnaise or cross-contamination

with meat juices or meat products was suspected.

Water

Several recent incidents show that both drinking

water and recreational water can serve as vehicles

for transmitting serotype O157:H7 infections.

The first and largest waterborne outbreak associated with this pathogen occurred in Missouri in

1989 (12). Of the more than 240 people infected, 32

were hospitalized, and four died. The source of the

outbreak was not identified, but backflow during a

water main break might have contaminated the

drinking water supply (12). Like most E. coli, serotype O157:H7 isolates are susceptible to the effects

of chlorine. Hence, adjustments in the chlorination

of the drinking water supply during repairs to the

water main might have prevented the outbreak (12).

An outbreak caused by serotype O157:H7 and S.

sonnei in 1991 may have involved recreational lake

water in the vicinity of Portland, Oregon. Of the 59

people affected, 21 (all children) were infected by

serotype O157:H7 (13). An epidemiologic survey

showed that those who became ill had swum in the

lake during the previous 3-week period. Transmission probably occurred when the swimmers swallowed lake water that was fecally contaminated by

other bathers. The lengthy period during which people became infected suggests that these pathogens

can remain viable in water for a long time, or that

the water was repeatedly recontaminated. Fecal

contamination of recreational water by bathers, especially small children, is not uncommon; however,

the contaminants are usually diluted quickly by the

large volume of water in recreational lakes, bays, or

rivers. That swallowing a small amount of lake

water can cause illness suggests that the pathogen

has a low infectious dose (13). This fact is already

well established for Shigella and seems to be consistent with recent epidemiologic data from foodborne

outbreaks associated with serotype O157:H7.

A similar incident, implicating water from a children’s paddling pool, was reported in Scotland in

1992 (14). Although epidemiologic evidence was not

conclusive, the available data suggested that a child

with diarrhea had played in the pool and fecally

contaminated the water with serotype O157. Because the pool water was not changed or disinfected,

it became the vehicle of infection for two other neighborhood children, who in turn infected others by

person-to-person contact.

Other vehicles of transmission

Recently, several other unique vehicles have been

implicated in foodborne outbreaks associated with

serotype O157:H7. A 1993 outbreak in an Oregon

restaurant was apparently caused by the consumption of cantaloupe or other items from the salad bar,

which were most likely cross-contaminated by meat

products during preparation. One study showed that

Synopsis

Emerging Infectious Diseases 48 Vol. 1, No. 2 — April-June 1995
serotype O157:H7 can survive and grow on salad

vegetables stored at 12°C and 21°C for up to 14 days

(15). An outbreak in the United Kingdom in 1991

was traced to the consumption of yogurt, which

infected 16 persons, 11 of them children (16). Although consumption of raw milk has caused past

outbreaks, serotype O157:H7 is susceptible to heat

treatment and thus does not usually survive the

pasteurization process. Even though the implicated

yogurt was prepared from pasteurized milk, the

milk might have become contaminated with serotype O157:H7 after pasteurization.

A puzzling incident was reported from northern

Italy, where 15 cases of HUS, caused by serotype

O157 and other EHEC serotypes, was recorded over

a 5-month period in 1993 (17). These cases occurred

in small towns scattered over a large area with little

apparent connection to each other; therefore, common food vehicles and exposure to cattle were eliminated as possible sources of infection. However, data

from the epidemiologic investigations suggested

that contact with live poultry or with chicken coops

may have been the source of infection, even though

no toxin-producing EHEC strains were isolated from

poultry feces. A recent study showed that inoculating

1-day-old chicks with strains of serotype O157:H7

resulted in rapid colonization of the cecal tissue of

the chicks. The chicks then became long-term (up to

11 months) shedders of serotype O157:H7, and this

microorganism was subsequently recovered from

the shells of their eggs (18). It is conceivable, therefore, that live poultry were the source of infection in

the outbreaks reported from northern Italy.

In December 1994, dry cured salami was implicated as the source of serotype O157:H7 in a disease

outbreak in the state of Washington (19). A prior

study showed that although isolates of serotype

O157:H7 do not grow in seeded sausage batter, they

can tolerate the acidity produced during sausage

fermentation and survive the drying and the cold

storage associated with the preparation of dry sausages (20). Fermented sausages can attain a pH as

low as 4.8 (20). The ability of serotype O157:H7

isolates to persist under these conditions is consistent with the acid-tolerant properties this organism

exhibited in the previously discussed studies with

apple cider (7) and mayonnaise (10).

Although the consumption of bovine products still

accounts for most of the serotype O157:H7 infections, the incidents described above show that other

food types can also serve as vehicles in transmitting

infections with this serotype.

Emergence of Phenotypic Variants 

Multilocus enzyme electrophoresis of E. coli

strains associated with enteric disease show that

serotype O157:H7 is in a well-defined group only

distantly related to other SLT-producing serotypes

(4,5). Recently, however, several phenotypic variants

of this serotype were isolated in Europe. Thus, in

addition to causing infections through food vehicles,

the problems associated with serotype O157:H7 are

compounded by the emergence of phenotypic variants, which may have an impact on diagnostic assays used to detect this pathogen.

The clonal nature of serotype O157:H7 has facilitated its phenotypic identification. Unlike other E.

coli, isolates of serotype O157:H7 do not ferment

sorbitol in 24 hours (21) and are negative in the

methyl-umbelliferyl glucuronide assay (22), which

measures glucuronidase activity (23). These phenotypes, especially the absence of sorbitol fermentation, are used extensively to distinguish isolates of

serotype O157:H7 from related bacteria. Isolation of

serotype O157:H7 from foods, on selective media,

such as hemorrhagic colitis agar (24) and cefiximetellurite sorbitol-MacConkey agar (25) is based on

the sorbitol phenotype. Similarly, sorbitol-MacConkey agar (26) is used in the clinical laboratory as

the primary screening medium to analyze patient

specimens for the presence of serotype O157:H7.

Prompt culturing of bloody stools with this agar has

been very effective in isolating serotype O157:H7

from stool specimens (1).

Although extremely useful, isolating and identifying the pathogen exclusively on the absence of

sorbitol fermentation has some limitations. Other

enteric bacteria, such as E. hermanii and Hafnia

spp., share similar phenotypes and resemble serotype O157:H7 on sorbitol-containing medium. Likewise, strains of O157, of non-H7 serotype that are

not pathogenic and do not ferment sorbitol have

occasionally been isolated from foods (27). Because

of the presence of phenotypically similar species

sorbitol negative isolates must be serologically confirmed with O157 and H7 antisera (28).

Though intended solely to select for serotype

O157:H7, sorbitol-containing media may also exclude the isolation of other pathogenic E. coli serotypes, many of which ferment sorbitol. It appears

that serotype O157:H7 is the predominant pathogenic serotype worldwide; however, a large number

of other serotypes also produce SLT (1,2). Although

many of these have not been implicated in disease

or are known to cause only nonbloody diarrhea, some

reports indicate that selected SLT-producing, nonO157:H7 serotypes may have caused cases of hemorrhagic colitis and HUS in Europe (29,30). In the

United States, disease caused by non-O157:H7 serotype is rare; however, a recent outbreak of bloody

diarrhea in Montana was suspected to have been

caused by a SLT-II-producing E. coli of serotype

O104:H21 (31).

A more relevant finding, and one that has

stronger implications regarding the reliance on sorSynopsis

Vol. 1, No. 2 — April-June 1995 49 Emerging Infectious Diseases
bitol phenotype for identifying pathogens, comes

from a recent study which showed that isolates of

serotype O157:H7 in sorbitol-containing foods can

mutate from a sorbitol-nonfermenting to a sorbitolfermenting phenotype (32). Moreover, the frequency

of isolation of sorbitol-fermenting O157 strains in

Europe appears to be increasing. In Germany, for

instance, strains of serotype O157:H-

 that produce

SLT-II have been isolated from HUS patients (33).

Unlike serotype O157:H7, these strains fermented

sorbitol and were positive in the methyl-umbelliferyl

glucuronide assay. Initially, these strains were considered atypical. However, other studies confirmed

that pathogenic, sorbitol-fermenting, serotype

O157:H-

 strains were fairly prevalent in HUS patients in central Europe (34). In another report,

serologic and biochemical characterization of 41

SLT-producing, O157 strains (including H7 and Hserotypes) determined that as many as 25% of the

isolates were sorbitol positive. Furthermore, there

was considerable variation among pathogenic serotype O157 isolates not only with respect to sorbitol

fermentation, but also with respect to other phenotypic characteristics (6). These variants are not detected by sorbitol-containing media and may not be

identified by the routine biochemical tests used to

characterize serotype O157:H7.

The notoriety of recent outbreaks has stimulated

the development of many new assays to detect serotype O157:H7; some of them may also be useful for

detecting phenotypic variants. Many of these assays

use molecular techniques, and some are commercially available. Several new molecular subtyping

methods have also been introduced. Although typing

methods will not be discussed here, such techniques

as ribotyping, pulsed-field gel electrophoresis (35),

lambda restriction fragment length polymorphism

(36), and others have been extremely useful in studying the epidemiology of serotype O157:H7 in foodborne outbreaks.

Phenotypic variants of serotype O157:H7 retain

the O157 antigen; hence, antibodies to O157 antigen

can be used to identify both serotype O157:H7 and

its variants. In the clinical laboratory, anti-O157

sera are used effectively in agglutination or latex

agglutination tests to rapidly screen or serologically

confirm isolates. Some anti-O157 antibodies have

also been coupled to magnetic beads and used to

selectively isolate this pathogen from foods (37) or

have been incorporated into enzyme immunoassays

to directly detect serotype O157:H7 in foods and

clinical specimens. The latter application of antiO157 sera, however, has had some drawbacks.

Many preparations of anti-O157 sera cross-react

with other bacteria, including Citrobacter freundii

(38), E. hermanii, and Yersinia enterocolitica O:9

(39). Moreover, the O157 antigen is present on other

non-H7 E. coli serotypes (6,40), many of which are

not pathogenic. For example, when anti-O157 serum

was used in an analysis of various food products,

nonpathogenic O157 isolates were found that neither produced SLT nor were of the H7 serotype (27).

Therefore, positive test results of food samples

tested with assays that use anti-O157 sera should

be confirmed by other methods. Pre-absorption of

diagnostic antisera to remove cross-reacting antibodies or the use of antibodies specific for other

non-O157 surface antigens of serotype O157:H7 may

reduce the frequency of serologic cross-reactions

(41).

Phenotypic variants also appear to retain the

pathogenicity of serotype O157:H7 (6,33); therefore,

assays specific for virulence factors are not affected

by the phenotypic variations described above. For

example, anti-SLT antibodies can be used to screen

fecal specimens for toxins, and SLT gene-specific

DNA probes and polymerase chain reaction (PCR)

can be used to identify all SLT-producing pathogens

regardless of phenotype. However, assays specific for

SLT or SLT genes do not provide sufficient data for

epidemiologic investigations and “trace-back” studies. More than 60 E. coli serotypes have been found

to produce SLT (1,2), and even strains from more

distantly related genera, such as C. freundii, reportedly produce SLT-II-like cytotoxins (42). Many of

these SLT-producing E. coli serotypes have not been

implicated in disease; therefore, the mere detection

of potential SLT-producing strains in foods or in

patients’ specimens by these assays is not conclusive

evidence that the bacteria caused the illness.

Some new assays do not have these limitations.

One PCR assay, designed as a mismatch amplification mutation assay, preferentially amplifies an allele in the uidA gene that is unique only to serotype

O157:H7, including its phenotypic variants of serotype O157:H-

 that are sorbitol and methyl-umbelliferyl glucuronide positive (43). Coupled with primers

specific for SLT genes, this multiplex PCR assay can

simultaneously identify isolates of serotype

O157:H7 and the type of SLT they encode (44).

Analysis of pure culture isolates showed that this

assay detected all SLT-producing serotypes and was

able to distinguish isolates of serotype O157:H7,

including the phenotypic variants.

Advantages of these new molecular methods include specificity, sensitivity, and the ability to detect

phenotypic variants of serotype O157:H7. However,

these assays are far too complex and costly for use

in the routine analysis of food or clinical specimens.

Furthermore, although the emergence of phenotypic

variants is of concern, they have only been observed

sporadically and are not prevalent worldwide.

Nonetheless, should the frequency of isolation or the

incidence of infection caused by these variants increase or should other SLT-producing serotypes of E.

coli become more firmly established as causative

Synopsis

Emerging Infectious Diseases 50 Vol. 1, No. 2 — April-June 1995
agents of illness, other media or assays may need to

be incorporated into existing diagnostic methods. In

the interim, the continued use of a sorbitol-containing medium such as sorbitol-MacConkey agar to

screen bloody stool specimens is a useful and economical laboratory procedure for the early diagnosis

of serotype O157:H7 infections.

Conclusions

Bovine products have most often been implicated

in foodborne infections with E. coli serotype

O157:H7. However, recent outbreaks indicate that

other food types may also serve as vehicles of transmission for this pathogen. Most notably, acidic foods

that were once thought to be of low risk can no longer

be considered safe because of the acid-tolerant properties of this bacterium. Most microbiologic media

and diagnostic assays have been designed specifically to detect serotype O157:H7. However, there is

phenotypic diversity within the serogroup. Should

these variants become more prevalent in infections,

the use of sorbitol medium alone may become inadequate in detecting the diversity of strains in this

pathogenic serotype.

Acknowledgments

The author thanks G.J. Jackson, FDA, for critical

review of this manuscript and L. Tomlinson, FDA,

for editorial assistance.

Dr. Feng is a research microbiologist with the Food

and Drug Administration in Washington, D.C. He was

a postdoctoral fellow in molecular biology at Purdue

University and a senior scientist at IGEN Inc. His

current research centers on developing rapid diagnostic

methods for detecting foodborne bacterial pathogens.

He is a member of the Microbiology Committee,

Association of Official Analytical Chemists

International, and serves as science advisor to

international health organizations and foreign

governments.

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Synopsis

Emerging Infectious Diseases 52 Vol. 1, No. 2 — April-June 1995