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Scientific Status Summary

Bacteria Associated
with Foodborne
This IFT Scientific Status Summary discusses Salmonella, Shigella,
Campylobacter, Listeria, and Vibrio species, and Yersinia enterocolitica,
Staphylococcus aureus, Clostridium perfringens, Clostridium botulinum,
Bacillus cereus, and Enterobacter sakazakii.

This Scientific Status Summary is an updated

review of the bacteria of primary significance
in foodborne disease, their significance as
pathogens, their association with foods, and
related control measures. The original publica-
A n estimated 76 million cases of foodborne illness occur each
year in the United States, costing between $6.5 and $34.9
billion in medical care and lost productivity (Buzby and
Roberts, 1997; Mead et al., 1999). In the United States, incidence of
tion appeared in the April 1988 edition of Food foodborne illness is documented through FoodNet, a reporting system
Technology. used by public health agencies that captures foodborne illness in over
13% of the population. Of the 10 pathogens tracked by FoodNet,
Salmonella, Campylobacter, and Shigella are responsible for most cases
of foodborne illness. When both the estimated number of cases and
mortality rate are considered for bacterial, viral, and parasitic cases of
foodborne illness, Salmonella causes 31% of food related deaths,
followed by Listeria (28%), Campylobacter (5%), and Escherichia coli
O157:H7 (3%) (Mead et al., 1999).
Data are only available for confirmed cases, and it is generally accepted
in the scientific community that the true incidence of foodborne disease is
underreported. Of the estimated 13.8 million cases of foodborne illness
due to known agents, roughly 30% are due to bacteria. The remaining cas-
es of known etiology are due to parasites in 3% of the cases and viruses in
67% of the cases (Mead et al., 1999). Because parasites (Orlandi et al.,
2002), E. coli O157:H7 (Buchanan and Doyle, 1997), and viruses (Cliver,
1997) have been addressed by previously published Scientific Status Sum-
maries, these pathogens are not discussed here. Enterobacter sakazakii, an
emerging pathogen of concern in infant formula, is a new inclusion in this
revised Scientific Status Summary.


Scientific Status Summary
Bacteria are the causative agents of microorganisms. Three types of bacteri- sulting in illness. Foodborne toxicoin-
foodborne illness in 60% of cases re- al foodborne diseases are recognized: fections result when bacteria present in
quiring hospitalization (Mead et al., intoxications, infections, and toxicoin- food, such as Clostridium perfringens,
1999). The international impact of fections. Foodborne bacterial intoxica- are ingested and subsequently produce a
foodborne illness is difficult to estimate. tion is caused by the ingestion of food toxin in the host.
However, about 2.1 million children in containing preformed bacterial toxin, Some pathogens reside in the intesti-
developing countries die due to diarrhe- such as the toxins produced by Staphy- nal tracts of normal, healthy animals
al-related illnesses annually. It is suspect- lococcus aureus and Clostridium botuli- and, in some instances, humans. Certain
ed that food or water is the vehicle for num, resulting from bacterial growth in microorganisms are ubiquitous in na-
many of these illnesses (WHO, 2002). the food. Foodborne infection, on the ture, occurring on soil and vegetation,
Because food is biological in nature other hand, is caused by ingestion of in animal wastes, and on animal carcass-
and is capable of supplying consumers food containing viable bacteria such as es. Human skin surfaces and nasal pas-
with nutrients, it is equally capable of Salmonella or Listeria which then grow sages harbor staphylococci. Water sup-
supporting the growth of contaminating and establish themselves in the host, re- plies may contain pathogens when con-

Table 1— Foodborne Disease in the United States, Including Estimated Annual Prevalence. Adapted from IFT (2000).
Bacteria Principal symptomsa Potential food contaminationa No. of illnessesb No. of deathsb

Bacillus cereus Diarrheal—watery diarrhea, abdominal Meats, milk, vegetables, fish 27,360 0
cramps and pain
Emetic—nausea and vomiting Rice products, starchy foods n/a n/a
Campylobacter spp. Watery diarrhea, fever, abdominal Raw chicken, beef, pork, shellfish, raw milk 1,963,141 99
pain, nausea, headache, muscle pain
Clostridium botulinum Weariness, weakness, vertigo, double Improperly canned or fermented goods 58 4
vision, difficulty swallowing and speaking
Clostridium perfringens Intense abdominal cramps, diarrhea Meat, meat products, gravies 248,520 7
Enterobacter sakazakii c Meningitis, enteritis Powdered infant formula 1:100,000 infantsc 20-50%c
Listeria monocytogenes Nausea, vomiting, diarrhea; influenza-like Raw milk, cheeses (particularly soft ripened 2,493 499
symptoms, meningitis, encephalitis; varieties), raw vegetables, raw meats, raw
septicemia in pregnant women, their and smoked fish, fermented sausages
fetuses, or newborns; intrauterine or cervical
infection that may result in spontaneous
abortion or stillbirth
Salmonella Typhi and Typhoid-like fever, malaise, headache, Raw meats, poultry, eggs, milk and 659 3
Salmonella Paratyphi abdominal pain, body aches, diarrhea, dairy products, fish, shrimp, yeast, coconut,
or constipation sauces, salad dressings (i.e., homemade items
containing unpasteurized eggs and no or
insufficient acidification for destroying pathogens)
Other Salmonella spp. Nausea, vomiting, abdominal cramps, fever, Raw meats, poultry, eggs, milk and 1,341,873 553
headache; chronic symptoms (e.g., arthritis) dairy products, fish, shrimp, yeast, coconut,
sauces, salad dressings (i.e., homemade items
containing unpasteurized eggs and no or
insufficient acidification for destroying pathogens)
Shigella spp. Abdominal pain and cramps; diarrhea; Salads (potato, tuna, chicken, macaroni) 89,648 14
fever; vomiting; blood, pus, or mucus raw vegetables, bakery products (e.g.,
in stools, tenesmus cream-filled pastries), sandwich fillings,
milk and dairy products, poultry
Staphylococcus aureus Nausea, vomiting, retching, abdominal Meat and meat products, poultry, egg 185,060 2
cramps, prostration products, salads (chicken, potato, macaroni),
cream-filled bakery products, milk and
dairy products

Vibrio cholera Serogroup 01 Mild watery diarrhea, acute diarrhea, Raw or recontaminated oysters, clams, crabs 49 0
rice-water stools
V. cholera Serogroup non-01 Diarrhea, abdominal cramps, fever, vomiting, Raw or recontaminated oysters, clams, crabs 49 0
nausea; blood or mucus-containing stools
Vibrio vulnificus Fever, chills, nausea, septicemia in individuals Raw or recontaminated oysters, clams crabs 47 18
with some underlying diseases or taking
immunosuppressive drugs or steroids
Other Vibrio spp. Diarrhea, abdominal cramps, nausea, Raw, improperly cooked or recontaminated n/a n/a
vomiting, headache, fever, chills shellfish or fish
Yersinia enterocolitica Fever, abdominal pain, diarrhea and/or vomiting Meats, oysters, fish, raw milk 86,731 2
Based on FDA/CFSAN (2003b).
Based on Mead et al. (1999). n/a indicates that no estimate was provided for this pathogen.
From WHO (2004).
taminated with fecal matter. Coastal wa- tices as major contributors to foodborne practices probably have the greatest
ters may also naturally harbor the illness (Altekruse et al., 1996; Meer and chances for success in controlling food-
pathogen Vibrio vulnificus. It is thus ob- Misner, 2000). For most of the patho- borne illness. The need for continual
vious how difficult it is to prevent one gens discussed in this Scientific Status education of consumers and all food
or more pathogens from contaminating Summary (Table 1), illness can be avoid- handlers concerning the significant haz-
foods. ed by heating and cooling foods to the ards associated with foodborne patho-
The presence of potentially life- appropriate temperatures, storing foods genic microorganisms and proper food
threatening pathogens in our environ- at the appropriate conditions for the handling procedures is evident. Regula-
ment, the ability of some of them to recommended period of time, hand- tory control over food handling in the
survive and/or proliferate under refrig- washing, and avoiding cross-contamina- home is not possible, but increased con-
eration and in reduced oxygen atmo- tion. Delicatessens, cafeterias, and res- sumer education could have a beneficial
spheres, and, for some pathogens, the taurants were responsible for 33% of effect.
low number necessary for causing dis- outbreaks (CDC, 2000b). Only one of
ease indicate the seriousness of the po- more than 1,300 outbreaks, including Salmonella
tential hazards with which we are faced. bacterial and viral, with known or un- Russell S. Flowers
The food industry implements a variety known etiology, was attributed to a
of effective control measures to limit “commercial product” in 2000 (CDC, Salmonella is a generic name applied
potential hazards. This generally begins 2000d). Proper handling, cooking, and to a group of nearly 2,000 biochemically
on the farm with the implementation of storage practices in foodservice opera- related serotypes responsible for food-
good agricultural practices. Some raw tions and in the home can prevent the borne illness.
products, such as poultry, are subject to majority of foodborne illnesses.
performance standards in spite of the In the foodservice sector, education Significance as a Pathogen
fact that the consumer will presumably of the food preparer and server, with The total number of cases of human
cook the product before consumption. emphasis on good personal hygiene, is salmonellosis have remained fairly con-
While all food manufacturers utilize the best preventive measure. Unfortu- stant between 1996 and 2002 (Figure 1),
control measures to ensure food safety, nately, the majority of foodservice although the serotypes causing illness
some food manufacturers are required workers are young (under 30 years of have changed (CDC, 2003a). Roughly
to create and follow a Hazard Analysis age), inexperienced, and stay on the job two to four million cases of foodborne
and Critical Control Point (HACCP) less than a year; thus, finding and edu- salmonellosis occur annually in the
plan. Critical control points identified cating these food handlers while they United States, and the estimated 1.3
through HACCP may include destruc- are actively working is difficult (Marth, million cases that occurred in 2000 cost
tion or inactivation of the relevant bac- 1985; National Restaurant Association, $2.4 billion in medical costs and lost
teria or their spores through the use of 2004). productivity (USDA/ERS, 2003). Be-
heat treatments (e.g., pasteurization, However, training programs such as tween 1988 and 1995 there were be-
canning), dehydration, freezing, refrig- Servsafe®, conducted through the Na- tween 40,000 and 50,000 reported, con-
eration, specialized packaging, and/or tional Restaurant Association Education firmed cases of salmonellosis annually;
approved antimicrobial preservatives. Foundation, and SuperSafeMark®, of- since 1997, that number has been below
Additionally, extensive quality control fered through the Food Marketing Insti- 35,000 (CDC, 2004; FDA/CFSAN,
procedures are maintained to ensure tute, have a positive impact on retail 2003b).
that these processes are effective. food safety practices (Cotterchio et al., The disease is grossly underreported
It is impossible, however, to create a 1998; Lynch et al., 2003; Mathias et al., because it is generally a self-limiting
risk-free food supply. While food manu- 1995). gastroenteritis which may be misdiag-
facturers and distributors employ neces- Several studies and reviews have nosed as intestinal influenza by the pa-
sary control measures to ensure the highlighted the contribution of chang- tient or the physician. As a consequence,
safety of food until it reaches the con- ing demographics in the United States estimates of the true incidence of dis-
sumer, all food handlers and consumers with the increased risk of foodborne ill- ease are based on assumptions derived
have the responsibility upon purchase ness (Knabel, 1995; Zink, 1997). The in- from epidemiological evidence. Clearly,
of the food to maintain these control crease in the elderly population and in- salmonellosis continues to be an impor-
measures until consumption. While dividuals with weakened immune sys- tant cause of foodborne disease world-
outbreaks associated with a particular tems underscores the need for rigorous wide.
commercially processed food receive food safety efforts, both on the part of Two clinical manifestations caused
widespread public attention, a much the food manufacturer and the consum- by Salmonella are recognized: enteric fe-
greater number of individual cases of er. Foodborne illnesses are more likely ver (a severe, life-threatening illness)
foodborne illness occurring in restau- to be life-threatening for the immune and the more common foodborne ill-
rants and in the home are not reported. compromised, the elderly, and individu- ness syndrome. In both cases, the re-
The Centers for Disease Control and als debilitated by underlying health sponsible microorganisms enter the
Prevention (CDC) reported that be- problems such as cirrhosis, hepatitis, body via the oral route.
tween 1993 and 1997, approximately hemachromatosis, etc. Enteric fever, commonly referred to
19% of foodborne illness outbreaks oc- Consumer education and increased as typhoid fever, is primarily caused by
curred in private residences. Numerous regulatory control of foodservice estab- one species, Salmonella Typhi, but other
surveys have highlighted inadequate lishments through inspection and strict salmonellae such as Salmonella
home food storage and handling prac- enforcement of proper food handling Paratyphi are potentially capable of pro-


Scientific Status Summary
ducing this syndrome. The illness is resulting from Salmonella infection is In some cases, gastroenteritis may be
commonly associated with foreign travel characterized by a self-limiting acute followed by extraintestinal invasion re-
and affects an estimated 800 people an- gastroenteritis. Contaminated food or sulting in enteric fever, which is more
nually (Mead et al., 1999). Although the water is the usual, but not the only, vehi- likely to occur in the very young, the
route of entry of the pathogen into the cle. The incubation period varies from aged, and debilitated patients.
body is primarily oral, the symptoms of six to 48 hr and generally falls within a
enteric fever are generally not elicited range of 12–36 hr. Variation in the incu- Association with Foods
through the intestinal tract. However, a bation time may be attributed to the size There are three main ways Salmonel-
short episode of vomiting and diarrhea of the infecting dose, the virulence (de- la can enter the food supply to cause ill-
sometimes occurs in the first day or two gree of pathogenicity) of the microor- ness. Animals harbor Salmonella, mak-
in typhoid fever. The onset times vary ganisms, the susceptibility of the host, ing meats, poultry, eggs, and milk often
considerably between typhoid and and the physicochemical composition of implicated vehicles. Salmonella, which
paratyphoid enteric fevers. Onset time the transmitting food. As few as 15 cells are introduced into the environment,
for typhoid is usually 8–15 days, seldom can cause illness (FDA/CFSAN, 2003b). possibly through manure and litter, may
as short as five days but sometimes as Symptoms include diarrhea, abdominal persist and contaminate fruits and vege-
long as 30–35 days; while onset time for cramps, vomiting, and fever, which gen- tables on the farm. Cross-contamination
paratyphoid fever tends to be shorter, erally last from one to seven days. How- in the food service environment or the
and may be so short as to suggest typical ever, the microorganisms may be excret- home, often between raw poultry and
food poisoning (Parker, 1984). The usu- ed in the feces for many weeks after ready-to-eat (RTE) products, such as
al symptoms of both are headache, mal- symptoms subside. Although the illness raw vegetables, can also cause salmonel-
aise, anorexia, and congestion of the is usually self limiting, there is a 15% losis.
mucous membranes, especially of the mortality rate in elderly who have devel- Some Salmonella are host-adapted
upper respiratory tract. Bacteremia gen- oped septicemia due to Salmonella dub- (e.g., Salmonella pullorum in poultry,
erally occurs in the first week of illness. lin, and a 3.6% mortality rate in nursing Salmonella dublin in cattle); however,
In a study of 1,138 cases, Coleman and home cases of Salmonella Enteritidis most Salmonella are not. Although any
Buxton (1907) reported positive blood (FDA/CFSAN, 2003b). Salmonellosis Salmonella is a potential pathogen for
cultures in 89% of patients during the may be confused clinically with staphy- humans, most foodborne salmonellosis
first week, 73% in the second week, 60% lococcal intoxication, but there are im- is caused by non-host-adapted sero-
in the third, 38% in the fourth, and 26% portant distinctions. Salmonella has a types.
after the fourth week. Arthritic symp- longer incubation period than staphylo- Much human salmonellosis is direct-
toms may emerge three to four weeks af- cocci (usually 12–36 hr vs. 2–4 hr) and ly related to human association with an-
ter infection in roughly 2% of the cases. is usually accompanied by fever, which is imals, both wild and domestic. Foods of
The 10% mortality rate of Salmonella absent in staphylococcal intoxication. animal origin are vehicles for salmonel-
Typhi and Salmonella Paratyphi is high And unlike Salmonella food poisoning, losis. Salmonella was isolated in 19–54%
compared to other Salmonella species the acute symptoms of staphylococcal of cattle carcasses, 1.9% of beef samples
(FDA/CFSAN, 2003b). food poisoning normally disappear at retail and 4.2% of retail chicken sam-
Typically, common foodborne illness within 24 hours. ples (Beach et al., 2002; Zhao et al.,
2001). In a review of Salmonella in
meats and poultry, Silliker and Gabis
(1986) introduced the problem as fol-
“The animal-to-man link is only one
factor in the epidemiology of human
salmonellosis. Contaminated red meat
and poultry provide a nidus (source of
infection) for Salmonella, which man
nurtures through mishandling. Further-
more, inedible parts of the animal are
processed to yield important compo-
nents of livestock feeds. As a result of
poor manufacturing practices (post-
processing contamination), these ren-
dered animal by-products become re-
contaminated with Salmonella, which,
in turn, are carried into the feeds. The
consumption of these feeds by livestock,
followed by animal-to-animal transmis-
sion, completes the Salmonella cycle.
This is not to suggest, however, that con-
Figure 1. Most Common Salmonella Isolates from Human Sources (data from CDC PHLIS Surveillance Data: taminated feeds are the only source of
Salmonella Annual Summaries); left axis: (g) Heidelberg, (#) Enteritidis, (•) Javiana, (!) Newport, (F) Salmonella in livestock. Epidemiological
Typhimurium; right axis: (-t—) total number of all Salmonella isolates. evidence indicates that there is a direct


link between the presence of Salmonella tion of milk destroys Salmonella and uncontaminated foods. Once contami-
in meat and poultry and human salmo- currently is the only effective means of nation occurs, the situation may be fur-
nellosis. Man induces salmonellosis control for milk. However, inadequate ther complicated by improper storage of
through improper food handling prac- pasteurization or contact with raw milk the product before serving (e.g., kept at
tices and perpetuates salmonellosis after pasteurization can result in con- room temperature, improperly refriger-
through recontamination of rendered taminated milk. In one pasteurized milk ated, or held in warmers within the
animal by-products, which are incorpo- outbreak in 1985, there were more than growth range for Salmonella).
rated into livestock feeds.” 16,000 laboratory-confirmed cases of Although responsible for fewer out-
Historically, egg products (dried, fro- salmonellosis and several deaths (Anon- breaks, contamination of foods by in-
zen or liquid eggs, with or without add- ymous, 1986). fected workers cannot be ignored as a
ed ingredients, as defined in the Egg Animal products are not the only cause of foodborne salmonellosis. Some
Products Inspection Act; U.S. Congress, sources of human salmonellosis. Pro- infected individuals may excrete Salmo-
1970) were a significant source of hu- duce can serve as a vehicle of Salmonella nella for weeks, months, and, occasion-
man salmonellosis in the United States. as well, becoming contaminated either ally, years with little or no evidence of
In 1990, the U.S. Dept. of Agriculture on the farm or through cross-contami- disease. Improper hygiene practices by
(USDA) required that eggs produced by nation with contaminated products. these individuals may lead to either con-
flocks previously implicated in human Consumption of produce contaminated tamination of foods or direct person-to-
disease be tested for Salmonella (FDA/ with Salmonella has recently caused sev- person contamination.
CFSAN, 2003b). Mandatory pasteuriza- eral outbreaks. In 2000, 361 individuals
tion of egg products was responsible for in England and Wales acquired salmo- Control Measures
greatly reducing eggs as a major cause of nellosis after eating lettuce, and al- Different control measures exist de-
salmonellosis, and consumer awareness though the lettuce appeared to come pending on the mode of contamination
of the need to refrigerate eggs also con- from one of three farms, investigators of the food. Reduction of the incidence
tributed in the decreased incidence of could not conclusively find the source of Salmonella contamination of foods
disease. However, since 1999, the inci- of contamination (Horby et al., 2003). requires a number of approaches to the
dence of Salmonella Enteritidis has re- The strain, S. enterica subsp. enterica se- problem, beginning at the farm and go-
mained stable. The microorganism is lo- rotype Typhimurium DT 104, is resis- ing right through to the kitchen.
calized inside eggs, making thorough tant to several antibiotics, and the in- Several approaches have been taken
cooking imperative. The CDC estimates crease in its prevalence poses challenges to reduce the carriage of Salmonella by
that 75% of Salmonella Enteritidis cases in treatment of the infection. Raw animals. Vaccinination of laying chick-
result from the consumption of raw or sprouts, particularly alfalfa and mung ens significantly reduced the percent of
undercooked grade A whole-shell eggs bean, have been involved in 15 salmo- eggs positive for Salmonella Enteritidis
(FDA/CFSAN, 2003b). This serotype nellosis outbreaks since 1995 (Thomas (Woodward et al., 2002). Other research
was the second most commonly report- et al., 2003). Seeds may be contaminat- has examined the effect of probiotics on
ed human serotype to the CDC in 2001. ed, and the warm, moist conditions for the intestinal microflora of chickens. In
A portion of these illnesses occurred as sprouting allow growth of the pathogen. this approach, the goal is to colonize the
a result of pooling raw shell eggs in in- On-farm contamination of cantaloupes chicken with known microorganisms to
stitutional or foodservice settings. The resulted in 24 cases of salmonellosis in “competitively exclude” Salmonella. Suc-
potential for temperature abuse or long 1997 (Mohle-Boetani et al., 1999). Con- cessful reduction in the percent of the
holding times, combined with the possi- tamination of cantaloupes on one farm flock positive for Salmonella was
bility of inadequate cooking, resulted in caused mulitstate outbreaks of salmo- achieved when the feed was supple-
the recommendation that institutions nellosis each spring between 2000 and mented with yeast (Line et al., 1998) or
use pasteurized egg products or pasteur- 2002 (CDC, 2002b). Since produce may when chickens were both sprayed with a
ized in-shell eggs instead of raw-shell be eaten raw, different control measures patented mucosal starter culture and fed
eggs (CDC, 2003c). are necessary to prevent illness when the the culture through water (Bailey et al.,
Consumption of raw milk may also pathogen is introduced on the farm. 2000).
cause human salmonellosis. In one While Salmonella may survive in In July 1996, USDA’s Food Safety and
study, Salmonella was isolated in 6.1% contaminated foods as a result of im- Inspection Service (FSIS) published
of bulk raw milk samples (Jayarao and proper cooking, it is more common that pathogen reduction performance stan-
Henning, 2001). Between 1972–2000, 16 cross-contamination of foods after dards for Salmonella. The performance
outbreaks of salmonellosis resulted cooking is the source of Salmonella. standard (percent positive) was estab-
from raw milk consumption (CDC, Foodservice workers or in-home food lished by collecting the average baseline
2003a). Milk-borne salmonellosis was preparers may transfer salmonellae from in the industry. Companies must use
particularly prevalent in Scotland, raw products to cooked or other uncon- HACCP and other measures to ensure
where, prior to 1983, the sale and con- taminated foods as a result of unsani- that the percent of their product that is
sumption of raw milk was common tary preparation practices (e.g., failure positive for Salmonella falls below this
(Sharp, 1986). Milk outbreaks in En- to wash hands) between handling of baseline. The performance standard has
gland and Wales were primarily associ- these foods. Salmonella can also be been expanded to include steers, cows,
ated with raw milk. The sale of raw milk transferred from contaminated raw broilers, hogs, and several related prod-
is legal in 27 states, although many have foods to equipment surfaces, such as ucts (FSIS, 1998). Between 1997 and
restrictions (CDC, 2003a; The Weston knives, cutting boards, and counter tops, 2003, FSIS reported a 66% decrease in
A. Price Foundation, 2003). Pasteuriza- and then from equipment to previously the presence of Salmonella in raw meat


Scientific Status Summary
and poultry (USDA, 2003). Due to the some death occurs during dehydrated and storing foods at the right tempera-
difficulty in completely eradicating Sal- storage, depending on the relative hu- tures.
monella from poultry, irradiation was midity (or aw) and storage atmosphere.
approved in 1999 as a means to control The rate of death of Salmonella in food Shigella
the microorganism as part of a HACCP preserved by reduced aw is increased at Russell S. Flowers
system (USDA, 1999). higher aw levels, temperatures, and oxy-
The most common method of elimi- gen levels (Genigeorgis and Riemann, Shigellosis, or bacillary dysentery, as
nating Salmonella from food products is 1979). In low-moisture products such as it is commonly known, is caused by bac-
heat processing. Salmonella is heat sensi- peanut butter and chocolate, Salmonella teria of the genus Shigella, which include
tive, and ordinary pasteurization or may remain for years, with little loss of S. dysenteriae, S. flexneri, S. boydii, and
cooking conditions are generally suffi- viability. S. sonnei (Figure 2) (Bryan, 1979). The
cient to kill it in high-moisture foods. As Moist, perishable products are gener- normal habitat for Shigella is the intesti-
with other microorganisms, the heat re- ally distributed under refrigerated or nal tract of humans and other primates.
sistance of Salmonella is markedly in- frozen conditions. Although freezing
creased as water activity (aw) decreases. and frozen storage can have some lethal Significance as a Pathogen
Current U.S. standards for milk pasteur- effects on Salmonella, it is well recog- Data suggest that Shigella is responsi-
ization result in a more than 1012-fold nized that Salmonella remain viable for ble for less than 10% of reported food-
reduction of viable Salmonella found in long periods of time in frozen foods and borne illnesses per year, infecting ap-
milk (Read et al., 1968). Minimum heat that survival is enhanced as the storage proximately 300,000–450,000 people
processes for pasteurization or cooking temperature decreases (Georgala and annually (FDA/CFSAN 2003b; Mead et
of most high-moisture products will Hurst, 1963). al., 1999). Although the primary mode
eliminate Salmonella from these prod- The presence of Salmonella in certain of transmission appears to be person-
ucts. Occurrence of Salmonella in such types of produce seems to result from to-person by the fecal-oral route (Feld-
processed products generally results introduction of the pathogen on the man and Riley, 1985), there have been
from post-processing contamination. farm. Contamination in these products, some documented cases of foodborne
In some cases, dry products may be which are typically not heated before shigellosis. The main source of Shigella
heat processed for the purpose of elimi- consumption, presents challenges to the involved in outbreaks is asymptomatic
nation of Salmonella. Ayres and Slos- food industry (CDC, 2002b; Thomas et carriers or persons recovering from dis-
berg (1949) and Banwart and Ayres al., 2003). For sprouts, chemical disin- ease. Shigella may persist in the intesti-
(1956) demonstrated the effectiveness fection of the seed coat is not mandato- nal tract for months (Bryan, 1978).
of dry-heat treatment on reducing Sal- ry, but is recommended by the Food and Symptoms of shigellosis include diar-
monella in pan-dried egg white. This Drug Administration (FDA). A survey rhea, abdominal pain, fever, and vomit-
work led to the eventual requirement of sprout producers in California found ing. The severity of the disease may vary
for dry-heat pasteurization of this prod- that most alfalfa sprout growers fol- from very mild to severe diarrhea with
uct (U.S. Congress, 1970). Similar treat- lowed FDA recommendations. Mung bloody stools, mucus secretia, and dehy-
ments have been applied to gelatin, ren- bean producers were less apt to follow dration. Reactive arthritis, hemolytic
dered animal by-products, nonfat dry the guidance (Thomas et al., 2003). An uremic syndrome and Reiters disease are
milk, and chocolate. outbreak involving 87 cases of Salmo- sequelae associated with shigellosis
Other than heat, the major manufac- nella mbandaka was linked back to (FDA/CFSAN, 2003b). Generally, food-
turing factors responsible for elimina- growers who did not disinfect seeds borne shigellosis is characterized by a
tion of Salmonella from food products (Gill et al., 2003). The recommended high attack rate, common-source epide-
are acidification and reduction of aw. level of chlorine treatment, 20,000 ppm, miology, and short incubation periods
Goepfert and Chung (1970) investigated still may not be sufficient to eliminate of 12–50 hr (FDA/CFSAN, 2003b).
the fate of Salmonella during sausage Salmonella, especially if they are local- Symptoms usually persist 3–14 days. In-
fermentation and concluded that the ized inside the sprout tissue, as Gandhi fection by some strains results in a 10–
combination of acidity and sodium et al. (2001) observed. Therefore, com- 15% mortality rate. Frequently, an as-
chloride was the principal reason for the pliance on the part of the grower, while ymptomatic carrier state may develop
demise of Salmonella during fermenta- worthwhile, does not guarantee a Sal- during convalescence, lasting from a few
tion. Similarly, Smittle (1977) reviewed monella-free product since chemical days to several months. Human-volun-
the literature on survival of Salmonella sanitizers may not be wholly sufficient teer studies indicate that ingestion of as
in mayonnaise and salad dressing and to eliminate the presence of Salmonella few as 10–100 microorganisms can in-
concluded that the principal factor re- in fruits and vegetables with natural duce illness (Morris, 1986).
sponsible for the death of salmonellae in openings and crevices (Beuchat and The disease is caused by invasion of
these products is acidity, but that a sec- Ryu, 1997). the intestinal mucosa. Enterotoxins,
ond important factor is reduction of aw When purchasing items likely to be classically referred to as Shiga toxins,
as affected by moisture, NaCl, and sugar contaminated with Salmonella, such as may be produced by S. dysenteriae and
concentration. These same factors are chicken, there are steps the food handler possibly by S. flexneri type 2A (Keusch
responsible for control of Salmonella in can take to prevent salmonellosis from et al., 1985). Shiga toxins block mRNA
a variety of fermented dairy, meat, and occurring in the home or food service transcription and induce apoptosis in
vegetable products. environments. These general food safety endothelial cells (Erwert et al., 2003;
Salmonella may survive for extended practices include avoiding cross-con- Thorpe et al., 1999).
periods in dehydrated foods. However, tamination, thoroughly cooking foods, Secondary infections with Shigella


occur frequently. Shigellosis can be a most other members of the family En- Control Measures
major problem in daycare centers, and terobacteriaceae, they are readily killed Shigellosis is a significant cause of
control is difficult due to the low infec- by most heat treatments employed in foodborne illness in both developed and
tious dose, unpredictable acquisition of the processing and preparation of foods, developing countries. Food microbiolo-
antimicrobial resistance, frequency of and do not survive well at pH below 4.5. gists should be aware that Shigella spe-
mild infections and carrier status, and However, studies on the survival of shi- cies can cause a rather severe form of
the frequency with which young chil- gella suggest that under certain selected foodborne illness (Smith, 1987) and
dren are transferred from one daycare conditions, they can survive for extend- that relatively low numbers of the mi-
center to another (CDC, 1984). The dis- ed periods in foods (Bryan, 1978). For croorganisms can cause disease. Prod-
ease is disproportionately common example, S. sonnei and S. flexneri have ucts suspected of foodborne illness
among the urban poor, immigrants, Na- been reported to survive at 25°C (77°F) should be analyzed for Shigella.
tive Americans, daycare centers, and in- in flour and in pasteurized whole milk Further studies are needed to deter-
stitutions (Bryan, 1978; Morris, 1986). for more than 170 days; in eggs, clams, mine the roles of the various toxins and
FoodNet data from 2003 captured 3,875 and shrimp for more than 50 days; in virulence factors in the disease process.
confirmed cases of shigellosis within the oysters for more than 30 days; and in The epidemiology of shigellosis should
13% of the population monitored. Ex- egg whites for more than 20 days. At be reevaluated, with particular emphasis
trapolated, this suggests almost 30,000 lower temperatures, such as 20°C (-4°F) on the environmental factors associated
cases would be confirmed in the U.S. and 0.5°C (32.9°F), survival for longer with the increasing incidence of S. son-
population (CDC, 2003b). In the early periods has been reported (Taylor and nei and S. flexneri. The waning incidence
1900s, S. dysenteriae and S. flexneri pre- Nakamura, 1964). of S. dysenteriae in U.S. epidemiological
dominated (Bryan, 1978). The pattern These laboratory data suggest that data clearly indicate that the major
of isolations suggests that prior to 1945, shigella may survive for extended peri- cause of shigellosis in developed coun-
direct fecal contamination of food and ods in foods and may grow under select- tries is infected food handlers. Thus,
water supplies may have been the pri- ed conditions. However, in practice, Shi- prevention and control of shigellosis re-
mary vector of disease. As socioeconom- gella is rarely isolated from processed quires either that infected humans not
ic and environmental sanitation (mu- products. Manufacturers do not rou- be permitted to handle foods or that
nicipal sewage disposal, safe water sup- tinely test their products, raw materials, they practice good personal hygiene
plies, and food hygiene) have improved, or processing environments for Shigella, such that, even if infected, the food does
the relative prevalence of S. sonnei has and there is no evidence to suggest that not become contaminated. Certainly,
increased. The explanation for this phe- routine testing is warranted. Most out- exclusion of infected individuals from
nomenon is not clear, but it may result breaks result from contamination of raw food handling is desirable. However,
from differences among the shigella in or previously cooked foods during prep- routine testing of food workers for Shi-
their ability to survive and grow outside aration in the home or in foodservice gella is neither practical nor necessary.
their human and animal hosts. establishments. Generally, the source of The principles necessary for control
contamination can be traced to a carrier of Shigella at the preparation and service
Association with Foods whose personal hygiene is poor (Bryan, level are the same as those necessary for
An estimated 20% of the total num- 1979). In underdeveloped countries, control of other more widely recognized
ber of cases of shigellosis involve food as harvesting of seafood from fecally con- pathogens such as Salmonella and
the vehicle of transmission (Mead et al., taminated waters and use of unsanitary Campylobacter. The increasing aware-
1999). The principal foods involved in water in food preparation may be ness of consumers and employees of
outbreaks include a variety of salads sources of disease. foodservice establishments of the po-
and seafoods (Morris, 1986) contami-
nated during handling by infected
workers (Bryan, 1978). Six separately re-
ported outbreaks in the United States
and Canada in 1998 involving S. sonnei
were traced back to parsley grown in
Mexico (Naimi et al., 2003). The pres-
ence of S. sonnei in commercially pro-
duced dip caused an outbreak on the
Pacific Coast in 2000. The product, mar-
keted under several brand names, was
ultimately recalled (CDC, 2000c). Im-
proper refrigeration of the contaminat-
ed product often contributes to illness.
After the initial infection from a con-
taminated food, the disease readily
spreads from person to person by the fe-
cal-oral route of transmission.
Shigella usually are considered to be
relatively fragile; i.e., they do not survive Figure 2. Relative contribution of species of Shigella causing foodborne illness; (g) S. boydii,
well outside the host (Bryan, 1978). Like (#) S. dysenteriae, (•) S. flexneri, (!) S. sonnei.


Scientific Status Summary
tential for foodborne diseases should do Association with Foods sibly by a mastitic infection of the bo-
much to reduce the incidence of Campylobacters are harmless inhab- vine udder. Fresh produce can be con-
shigellosis in the developed countries. In itants of the gastrointestinal tract of a taminated by fecal-laden irrigation wa-
the developing countries, control of variety of wild and domestic animals. ter, infected harvesters with poor hy-
shigellosis, as always, will depend on Studies have revealed that as many as gienic practices, or tainted processing
improved hygiene and waste-handling 30–100% of poultry, 40–68% of cattle, water. Although eggs have rarely been
practices. and up to 76% of swine carry C. jejuni linked to outbreaks of Campylobacter
or C. coli in their intestinal tracts (Beach enteritis, C. jejuni has been isolated
Campylobacter jejuni et al., 2002; Harvey et al., 1999). For this from the surface of eggs laid by Campy-
and other species reason, the microorganism is often asso- lobacter-infected hens (Doyle, 1984;
Michael P. Doyle ciated with unprocessed foods of animal Finch and Blake, 1985).
origin. Surveys of U.S. retail fresh red C. jejuni and other campylobacters
Originally considered a pathogen meat and poultry show that 12–35% of are not likely to grow in foods that re-
principally of veterinary significance, turkey, 64% of chicken, 2–5% of pork, main edible because the organisms: (1)
Campylobacter jejuni (formerly known 0–5% of beef, 8% of lamb and 9% bulk will not grow below 30°C (86°F); (2) re-
as Vibrio fetus) was known to cause tank raw milk contained C. jejuni and/ quire microaerophilic (low concentra-
abortion in sheep. Other enteric campy- or C. coli (Jayarao and Henning, 2001; tions of oxygen, ideally 5–10%) condi-
lobacters that may be transmitted Logue et al., 2003; Stern et al., 1985; tions for growth; (3) grow slowly even
through food include C. coli, C. lari, and Zhao et al., 2001). It is estimated that under optimal conditions; and (4) are
C. upsaliensis, although many other spe- roughly half of all cases of Campylo- not good competitors with other micro-
cies have been identified. bacter entertitis are associated with un- flora. Additionally, C. jejuni is a very
dercooked chicken or cross-contamina- fragile microorganism, being sensitive to
Significance as a Pathogen tion with raw chicken (FDA/CFSAN, drying, normal atmospheric concentra-
Following the development of proce- 2003b). In a 1996 outbreak, raw lettuce tions of oxygen, storage at room tem-
dures for detecting campylobacters in served as the vehicle for Campylobacter perature, acidic conditions, disinfec-
stool specimens, C. jejuni became recog- infections, presumably after contact tants, and heat. Because the microor-
nized as a leading cause of acute bacteri- with raw chicken (CDC, 1998). Other ganism is quite sensitive to stressful en-
al gastroenteritis in humans. Recent evi- foods implicated as vehicles of out- vironmental conditions when outside of
dence suggests that Campylobacter caus- breaks include raw milk, raw beef, the host’s digestive tract, campylobacters
es 2–4 million cases per year in the clams, and cake (likely contaminated by are not likely to be a problem in pro-
United States (FDA/CFSAN, 2003b; a C. jejuni-infected food handler). Con- cessed foods that receive a pasteuriza-
Mead et al., 1999). Common symptoms sumption of C. jejuni-contaminated raw tion treatment or are dehydrated. How-
of Campylobacter enteritis include pro- milk from an organic dairy farm made ever, the microorganism is often associ-
fuse watery or sticky diarrhea (some- 75 Wisconsin residents ill in 2001 ated with and transmitted by raw, refrig-
times containing blood), abdominal (CDC, 2002c). Incompletely pasteurized erated foods of animal origin.
cramps, headaches, muscle pain, and milk was responsible for an outbreak of
nausea. The mortality rate is low (0.1%) Camplyobacter enteritis affecting 110 Control Measures
and often occurs in susceptible popula- people in the United Kingdom (Fahey, C. jejuni infections can be prevented
tions such as the elderly, young, or im- 1995). Although C. jejuni is responsible by properly pasteurizing or cooking
munocompromised (FDA/CFSAN, for more foodborne illness than C. coli, foods (especially foods of animal origin)
2003b). Roughly 25% of cases experi- the significance of the latter should not and avoiding cross-contamination of
ence relapses. Although sequelae such as be overlooked. Estimates from studies in cooked or RTE foods by utensils, equip-
Guillain-Barré syndrome, meningitis, England and Wales revealed that ap- ment, or cutting surfaces that are not
recurrent colitis and acute cholecystitis proximately 25,000 cases of foodborne properly cleaned and disinfected after
are uncommon, campylobacter is asso- illness were caused by C. coli in the year contact with fresh, uncooked meats and
ciated with more than 30% of cases of 2000 (Tam et al., 2003). Outbreaks of foods likely to be contaminated with the
Guillain-Barré (FDA/CFSAN, 2003b; Camplylobacter enteritis are generally microorganism. Pasteurization will
Mead et al., 1999). Human volunteer small; however, untreated surface water eliminate viable campylobacters in milk.
and retrospective studies of food-associ- used in municipal water supplies has Use of potable irrigation and processing
ated outbreaks of Campylobacter enteri- been responsible for large outbreaks in- water and safe food handling practices
tis revealed that ingesting relatively volving thousands of individuals. by harvesters are important to the safety
small numbers (only a few hundred The principal route by which C. jeju- of produce. Although C. jejuni does not
cells) of C. jejuni can produce illness. ni contaminates food is through fecal survive well in foods, refrigeration pro-
Symptoms manifest after an incubation contamination by Campylobacter-infect- longs survival. Freezing food will sub-
period of two to five days, and generally ed carriers. Raw meats and poultry be- stantially reduce the initial Campylo-
last 7–10 days. Treatment with erythro- come contaminated during processing bacter population; however, a small
mycin can decrease an individual’s du- when intestinal contents contact meat number of survivors may remain viable
ration of shedding the microorganism surfaces. Raw milk may be contaminat- for many months (Moorhead and
(FDA/CFSAN, 2003b). ed by contact with bovine feces or pos- Dykes, 2002). Testing foods for the pres-


ence of Campylobacter is difficult since carriers of virulent types of Yersinia pathogenic strains in foods may explain
enrichment with antibiotics is necessary (Zen-Yoji et al., 1974). why there are relatively few reported
and cells must be grown in an environ- Not surprisingly, because swine are food-associated outbreaks of yersiniosis.
ment of 5% O2 and 10% CO2. the primary reservoir of virulent types The microorganism is one of a few
of Y. enterocolitica, illness has been asso- foodborne pathogens that can grow at
Yersinia enterocolitica ciated with the consumption of pork in- refrigeration temperatures. Studies in
Michael P. Doyle testines. The product, known as chitter- raw pork revealed that within 10 days at
lings, is traditionally eaten during the 7°C (44.5°F) the microorganism could
Yersinia enterocolitica is not a fre- winter holidays, generally by African grow from a few hundred cells to mil-
quent cause of human infection in the Americans, and the incidence of yersini- lions/g (Hanna et al., 1977). Hence, re-
United States; illness is more common osis increases in December for the con- frigeration, which traditionally has been
in Northern Europe, Scandinavia, and suming population. Infants and chil- an important means of controlling the
Japan. dren are most often affected, largely be- growth of foodborne pathogens, is not
cause of caretakers who do not properly an effective method for controlling Yers-
Significance as a Pathogen wash their hands between preparing inia.
Although CDC estimates that there chitterlings and feeding young children,
are 17,000 cases of yersiniosis, the infec- or practice adequate kitchen hygiene Control Measures
tion caused by Y. enterocolitica, per year, (Jones et al., 2003; Lee et al., 1991). For Y. enterocolitica is sensitive to heat
less than 7,500 total cases were reported epidemiological purposes, these cases (e.g., pasteurization at 71.8°C for 18
between 1990 and 1999 (Ackers et al., are not reported as foodborne illness, sec), sodium chloride (5%), and high
2000; FDA/CFSAN, 2003b). When the since the food is not ingested, but clearly acidity (pH 4.0), and will generally be
microorganism is involved in illness, inactivated by environmental conditions
which typically manifests 24–48 hr after that will kill Salmonella (Robins-
ingestion, the symptoms can be quite se-
vere; but fatalities are rare. The infective
Y. enterocolitica is com- Browne, 1997). However, since Yersinia
will grow at refrigeration temperatures,
dose is unknown. Yersiniosis occurs monly present in foods; cold storage can be a means of selective-
most commonly in the form of gastro- ly promoting growth of the microorgan-
enteritis. Children are most severely af- however, with the excep- ism in foods. Therefore, it is important
fected with symptoms of intense ab- to eliminate the microorganism from
dominal pain (often mimicking appen- tion of pork, most isolates foods (especially pork, milk, and foods
dicitis), diarrhea, fever, and vomiting. that may have direct or indirect contact
Symptoms of pseudoappendicitis have from foods are avirulent. with porcine waste) by pasteurization or
resulted in many unnecessary appendec- cooking. Care should be taken to avoid
tomies in children. The illness has also cross-contamination of processed, RTE
been misdiagnosed as Crohn’s Disease the porcine intestines served as the foods with pork and porcine wastes, as
(FDA/CFSAN, 2003b). Fatality from source of the pathogen. well as animal and human fecal contam-
gastroenteritis is rare, and recovery is A study of bulk tank milk revealed ination.
generally complete within one or two that 6.1% of samples were positive for Y.
days. Arthritis has been identified as an enterocolitica. Further testing deter- Listeria monocytogenes
infrequent but significant sequela in 2– mined that all strains were virulent (Ja- and other Listeria species
3% of Y. enterocolitica infection cases. yarao and Henning, 2001). Chocolate Originally authored by Joseph Lovett
Other syndromes may include mesen- milk, pasteurized milk, and tofu packed and Robert M. Twedt. Reviewed by
teric lymphadenitis, terminal ileitis, in unchlorinated spring water have all Stephanie Doores.
erythema nodosum, septicemia, and been vehicles of outbreaks of yersiniosis
meningitis. (Ackers et al., 2000). The precise mode Prior to the 1980s, listeriosis, the dis-
of transmission was not determined, ease caused predominantly by Listeria
Association with Foods but in each situation there was thought monocytogenes, was primarily of veteri-
Y. enterocolitica is principally a to be a lack of sanitary practice or defi- nary concern, where it was associated
zoonotic bacterium that has been isolat- ciencies in good manufacturing practic- with abortions and encephalitis in sheep
ed from a variety of animals. However, es. Circumstantial evidence suggests and cattle. Interestingly, evidence indi-
most animal isolates, with the exception that porcine waste may have been the cates that veterinary listeriosis was fre-
of swine isolates, are not human patho- original source of Y. enterocolitica in- quently foodborne. As a result of its
gens. Swine is an important and the volved in some of the food-associated wide distribution in the environment,
principal reservoir for virulent strains of outbreaks (Toma and Deidrick, 1975; its ability to survive for long periods of
Y. enterocolitica, with such isolates often Wauters, 1979). time under adverse conditions, and its
recovered from the tonsils and tongues Y. enterocolitica is commonly present ability to grow at temperatures as low as
of apparently healthy animals (Doyle et in foods; however, with the exception of –0.4°C, Listeria has since become recog-
al., 1981). A study in Japan revealed that pork, most isolates from foods are avir- nized as an important foodborne patho-
rats in slaughterhouse areas may also be ulent. The infrequent presence of gen (ICMSF, 1996).


Scientific Status Summary
Significance as a Pathogen immunocompromised, newborn, or crops dangerous. The use of sludge for
Immunocompromised humans are very young (FDA/CFSAN, 2003b). Fever fertilization of edible crops is equally
highly susceptible to virulent Listeria. is a common symptom, and other com- hazardous.
The microorganism causes approxi- plaints may vary from nonspecific fa- L. monocytogenes can grow in the pH
mately 1,600 cases of listeriosis, result- tigue and malaise to enteric symptoms. range of 4.39–9.4 in a good growth me-
ing in approximately 415 deaths annual- Forms of listeriosis involving the dium (ICMSF, 1996). Environments
ly (FDA/CFSAN, 2003b). Only the central nervous system include meningi- with pH values outside that range are
hemolytic species of Listeria (L. monocy- tis, encephalitis, and abscesses. The clin- unfavorable for survival. The microor-
togenes, L. seeligeri, and L. ivanovii) are ical course for meningitis develops and ganism has readily survived the pH 5
associated with pathogenicity. Of these, progresses suddenly, and the fatality rate environments of cottage cheese and rip-
only L. monocytogenes is consistently can be as high as 70%. Localized forms ening Cheddar cheese, and was detect-
pathogenic; L. ivanovii has rarely been of listeriosis, which are rare, include en- able in the latter product (pH 5.0–5.15)
reported to be involved in human pa- docarditis, endophthalmitis, and osteo- for more than one year (Ryser and
thology, and L. seeligeri was reported myelitis, with the involvement of other Marth, 1987).
only once to be the cause of meningitis sites such as skin, spleen, gall bladder, Listeria is salt tolerant, growing to
in a non-immunocompromised adult. and lymph nodes. All forms of listeriosis levels of visible turbidity in the labora-
Listeriosis is a very serious and often are more likely to accompany immuno- tory media Tryptic Soy Broth (pH 5.0)
fatal infection primarily affecting the after 41 hr at 25°C in presence of 10%
elderly and perinates. However, gas- sodium chloride (ICMSF, 1996). How-
trointestinal illness has recently been
recognized as a possible manifestation
The first reported outbreak ever, 12.5% sodium chloride inhibited
the growth of L. monocytogenes at pH
of ingestion of Listeria. Unlike the more of foodborne listeriosis 6.0 between 8 and 30°C (Razavilar and
severe form of listeriosis, gastrointesti- Genigeorgis, 1998). Listeria is reported
nal illness, which generally results more occurred between March to survive for three months in dry fod-
than 12 hr after ingestion, primarily af- der and more than six months in dry
fects seemingly healthy adults. In some and September 1981. straw. Dry feces have been reported to
instances, this type of illness is associated maintain viability of the microorganism
with the consumption of large doses of L. for more than two years (Gray, 1963),
monocytogenes (Dalton et al., 1997). compromised states, whether natural (as and survival in soil for up to 295 days
In humans, ingestion of as few as in pregnancy, or in the elderly) or in- has been recorded. Listeria is relatively
1,000 cells of the bacteria, which then duced as a result of medical treatment resistant to drying, as demonstrated on
invade macrophages, may be marked by (such as with corticosteroids). Individu- glass beads and tile surfaces. Survival is
a flu-like illness (malaise, diarrhea, and als using antacids or cimetidine may temperature dependent, with lower tem-
mild fever). This enteric phase, however, also be more susceptible to infection, peratures enhancing survival (Dickgie-
may be without symptoms, or so mild because of changes in stomach acidity. ber, 1980; Welshimer, 1960), an impor-
as to go unnoticed. A carrier state may Listeriosis is often treated with penicillin tant factor in Listeria’s significance in
develop. Between 1–10% of symptom- or ampicillin (FDA/CFSAN, 2003b). the food chain.
less persons may be excretors of L. The first reported outbreak of food-
monocytogenes (FDA/CFSAN, 2003b). Association with Foods borne listeriosis occurred between
Identification of Listeria as the causative Listeria is ubiquitous in nature, oc- March and September 1981. Coleslaw
agent of foodborne illness is complicat- curring in soil, vegetation, and water was implicated as the cause of 34 cases
ed by the high carrier rate in humans (Beuchat and Ryu, 1997; Coyle et al., of perinatal listeriosis and seven cases of
and must be isolated from the food for 1984; Pearson, 1970), and therefore is adult listeriosis in the Maritime Prov-
confirmation (FDA/CFSAN, 2003b). frequently carried by humans and ani- ince of Nova Scotia. Perinatal cases were
Following invasion of macrophages, mals. Listeria can survive for long peri- characterized by acute febrile illness in
virulent strains of Listeria may then ods in both soil and plant materials. In- pregnant women, followed by spontane-
multiply, resulting in disruption of these gestion of contaminated silage by rumi- ous abortion (five cases), stillbirth (four
cells and septicemia. In this stage, occur- nants has been linked to the occurrence cases), live birth of a seriously ill prema-
ring five days to three weeks after inges- of Listeria in milk (Donnelly, 1987). ture or term infant (23 cases), or live
tion, the microorganism has access to all Biological oxidation during wastewa- birth of a well infant (two cases). The fa-
body areas and may involve the central ter treatment favors the growth of Liste- tality rate for infants born alive was
nervous system, the heart, the eyes, or ria in sewage. Sludge provides a favor- 27%. The outbreak strain was isolated
other locations, including the fetuses of able environment for survival and from two unopened packages of cole-
pregnant women (FDA/CFSAN, 2003b). growth of L. monocytogenes for many slaw from the plant but was not cul-
The stage of pregnancy upon exposure months (Guenich and Muller, 1984). L. tured from the manufacturing plant en-
of the fetus to the microorganism deter- monocytogenes in concentrations of 103– vironment. The incriminated coleslaw
mines the outcome for the fetus (abor- 104 cells/mL have been found associated was traced to a farm where the cabbage
tion, stillbirth, or neonatal sepsis). The with sewage plant effluents, while sew- was grown in fields fertilized with sheep
perinatal and neonatal mortality rate is age sludges have shown higher concen- manure. Two of the sheep on the farm
80% (FDA/CFSAN, 2003b). Death is trations. This makes the use of sewage had previously died from listeriosis
rare in healthy adults; however, the mor- plant effluent or waters receiving sewage (Schlech et al., 1983).
tality rate may approximate 50% in the plant effluent for irrigation of edible Although listeriosis is more com-


monly reported as sporadic cases, of the FDA and USDA have a “zero toler- raw and finished product, whether these
which about 20% result from the con- ance” (absence in 25 g) for L. monocyto- cross-connections be humans, equip-
sumption of unheated hot dogs and un- genes in RTE foods. The 2003 risk as- ment, water, air, or the piping arrange-
dercooked chicken, there have been sessment prepared jointly by the agen- ment within the plant. If a personnel
many outbreaks involving a variety of cies estimated the relative risk of listeri- practice or movement within the plant
foods (FDA/CFSAN and USDA/FSIS, osis in 23 categories of RTE foods. The provides contamination potential, it
2003). Hot dogs and deli meats contam- agencies report that the results of the should be eliminated or modified. If a
inated with L. monocytogenes serotype risk assessment will be used to focus piping arrangement can, under some
4b caused a 1998–1999 outbreak affect- control efforts on high-risk foods (FDA/ circumstances, transport potentially
ing 101 individuals in 22 states (FDA/ CFSAN and USDA/FSIS, 2003). In terms contaminated material from the “dirty”
CFSAN and USDA/FSIS, 2003). In 2002, of risk per serving, deli meats ranked as area or process to the finished product
63 cases of listeriosis, of which three having the highest risk. area, it should be eliminated, no matter
were perinatal, resulted from the con- Because of the link between dairy how many valves intervene. Not even
sumption of sliced deli meat in eight foods, particularly milk, and L. monocy- the air in the potentially contaminated
Northeastern states. This type of food togenes, the adequacy of pasteurization area should be shared with the finished
product was also responsible for an out- temperatures and times to inactivate L. product area.
break in 2000 affecting 29 people in 10 monocytogenes were intensively studied. Thus, the sanitation regimen of the
states (CDC, 2000a). Scientific consensus on this subject entire plant must be under constant
The soft cheeses are now infamous holds that the risk of post-pasteuriza- scrutiny and evaluation. Even with strict
for their susceptibility to contamination tion contamination is a far more serious sanitation practices, all open product
with L. monocytogenes, presumably due threat than survival of the microorgan- processes should be considered poten-
to the use of raw milk or because of ism to pasteurization heat treatment tial contamination points, and careful
post-pasteurization contamination. Not (63°C for 30 min or 71.7°C for 15 sec). scrutiny, including microbiological
only is the manufacturing process open Two studies by Bunning et al. (1986, analysis, should be a part of the quality
to contamination, but the cheese can 1988) failed to support the hypothesis control practice.
serve as a growth environment where L. that an intracellular location of the bac- Concern cannot stop at the point of
monocytogenes can multiply during the teria in polymorphonuclear leucocytes packaging; storage and distribution
storage period, even under refrigeration may confer heat resistance and allow practices must also be evaluated as part
at 4°C (39.2°F). Concentrations of Liste- survival during pasteurization. Heat of an effective quality control program.
ria as great as 106 cfu/g have been noted. shock at 42 or 48°C for up to 60 min did The ability of L. monocytogenes to with-
Mexican-style cheese made with raw not confer significantly increased ther- stand harsh environmental conditions
milk was implicated in two separate motolerance at 52 or 57.8°C (Bunning such as pH extremes, heat, and freezing
outbreaks, one in 1984 causing 142 ill- et al., 1990). requires special considerations when
nesses, and one in 2000–2001 resulting The control of Listeria in food prod- planning for storage and distribution.
in 12 cases. The mortality rate was ucts begins at the lowest level in the Surviving microorganisms can grow in
33.8% and 41.7%, respectively (CDC, processing chain—at the raw product products under conditions that would
2001; Linnan et al., 1988). source. The growing environment inactivate other microorganisms. Addi-
While association of listeriosis with should be kept free of the opportunity tionally, L. monocytogenes is capable of
raw milk consumption is not rare, it is for potential contamination. Waters sus- doubling in number each 1.5 days when
infrequent and sporadic. The results of pected of contamination by Listeria, refrigerated at 4°C (39.2°F). This is of
surveys of raw milk for L. monocytogenes sewage plant effluent, and sewage slud- particular concern since more than half
show that the presence of the microor- ges should not be used to produce crops the home refrigerators surveyed in a
ganism in raw milk is common in the that will be eaten without cooking or 1999 Audits International study exceed-
United States and Europe (Dominguez that will become an ingredient of a ed 39°F (FDA/CFSAN and USDA/FSIS,
Rodriguez et al., 1985; Lovett et al., product that will be eaten raw. Contain- 2003).
1987). The 2003 risk assessment con- ers, cartons, boxes, tankers, trucks, or
ducted jointly by FDA/CFSAN and rail cars used to transport the product Vibrio species
USDA/FSIS pooled the data of 45 stud- to the process plant should be frequent- Joseph M. Madden
ies, which showed an overall positive ly cleaned.
rate of 4.1% (FDA/CFSAN and USDA/ At the plant, the raw product itself The three Vibrio species of primary
FSIS, 2003). The presence of L. monocy- becomes a source of contamination for significance in foodborne illnesses are V.
togenes in pasteurized milk in the United the environment. Product flow must be cholerae (serogroups O1, non-O1, and
States is rare, with an average percent designed to segregate Listeria-free food recently, O139), V. parahaemolyticus,
positive of 0.4% in more than 10,000 from potentially contaminated environ- and V. vulnificus. Another species, V.
samples tested in 30 studies conducted ments by control of the product pro- mimicus sp. novo (Davis et al., 1981),
worldwide (FDA/CFSAN and USDA/ gression through the plant in a manner formerly included in the species V. chol-
FSIS, 2003). that separates “clean from dirty,” or pro- erae, also is a recognized pathogen.
cessed from raw. Personnel, too, must
Control Measures have their movements within the plant Significance as a Pathogen
Because of the severity of listeriosis restricted depending on their exposure An estimated 10.1 Vibrio infections
and the ability of the microorganism to to potential contamination. There per million adults who consume raw
grow at refrigeration temperatures, both should be no cross-connections between oysters occur annually in the United


Scientific Status Summary
States (FDA/CFSAN, 2001). Between tion. V. cholerae non-O1 can cause sep- risk assessment estimated that only 15%
1981 and 1994, V. parahaemolyticus and ticemia in susceptible individuals (those of illnesses are caused by the consump-
V. cholerae non-O1 caused roughly the with other underlying diseases such as tion of raw oysters containing >10,000
same number of illnesses, but gastroen- cirrhosis, diabetes, and hemachromato- viable V. parahaemolyticus cells.
teritis was the common symptom for sis, or those on immunosuppressive V. vulnificus is primarily associated
the former, whereas septicemia occurred therapy) via the gastrointestinal tract or with serious wound infections and life-
more often in cases of the latter (FDA/ wound infections. Septicemia may be threatening primary septicemia (Blake et
CFSAN, 2001). V. vulnificus was the accompanied by nausea, but is usually al., 1979). Primary septicemia is a very
strain most often responsible for illness, not accompanied by diarrhea. Fever, serious disease with a 50% fatality rate.
which usually manifested as septicemia chills, and nausea may result from the Most cases identified also had preexist-
(FDA/CFSAN, 2001). cellulitis occurring with the wound in- ing liver disease (Blake et al., 1979);
V. cholerae is the bacterium responsi- fections. however, others have been healthy indi-
ble for cholera epidemics and outbreaks. Only about 3% and 0.2–0.3% of viduals (Tison and Kelly, 1984). The se-
Three groups of V. cholerae strains are strains of V. parahaemolyticus are vere wound infections, which may re-
recognized: serogroups O1, O139, and pathogenic on the West Coast and Gulf quire amputation or result in death,
non-O1. V. cholerae O1 is the serogroup Coast, respectively (FDA/CFSAN, usually occur after trauma and exposure
traditionally associated with cholera 2001). Pathogenic strains of V. para- to marine animals or the marine envi-
cases, involving severe, watery diarrhea haemolyticus are responsible for out- ronment (Blake et al., 1979). The mor-
through the action of cholera toxin breaks of acute gastroenteritis, with tality rate associated with wound infec-
(Farmer et al., 1985). The serogroup is symptoms of nausea, vomiting, abdom- tions, 7%, is much lower than that asso-
divided into the Classical and El Tor inal cramps, low-grade fever, chills, and ciated with septicemia.
biotypes (Peterson, 2002). A new sero- V. mimicus is associated with a mild
type of V. cholerae, O139, emerged in In- gastrointestinal illness similar to V. chol-
dia in 1992 and spread to neighboring era non-O1, usually occurring after the
countries. V. cholerae O139 also causes Approximately 10–20% of consumption of raw seafood, particular-
cholera, but many secondary infections ly oysters (Shandera et al., 1983). The
are asymptomatic (Albert, 1996). the population consumes microorganism is probably distributed
In volunteer feeding studies of sero- worldwide in countries situated on an
group O1, ingestion of 106 cells caused
raw seafood annually and ocean, and its ecology may be similar to
illness. The incubation period is typical-
ly from six hours to five days (FDA/CF-
is at increased risk of that of V. cholerae non-O1 (Farmer et al.,
SAN, 2003b). Symptoms of severe chol- infection by Vibrio species.
era include massive diarrhea with large Association with Foods
volumes of “rice-water” stool (clear flu- Approximately 10–20% of the popu-
id with sloughed-off dead intestinal lation consumes raw seafood annually
cells). If left untreated, severe dehydra- diarrhea (usually watery, sometimes and is at increased risk of infection by
tion and death can occur. The massive bloody) that begin 12–96 hr after inges- Vibrio species (FDA/CFSAN, 2001).
water loss associated with V. cholerae in- tion. The disease is generally mild and Roughly two-thirds of cases are associat-
fections has been attributed to the pro- self-limiting, lasting from two hours to ed directly or indirectly with seafood;
duction of toxin by the microorganisms 10 days, but progression to septicemia i.e., either by consumption of raw sea-
that adhere to and colonize the small in- can be fatal (Farmer et al., 1985; FDA/ food or by consumption of seafood
testine of infected individuals. The chol- CFSAN, 2001). which has been recontaminated after
era toxin causes massive fluid loss from In Japan, where ingestion of raw sea- cooking. Oysters are commonly associ-
cells lining the intestinal tract, and the food is common, V. parahaemolyticus is ated with Vibrio contamination. In a
familiar rice-water stool. Diarrhea can an extremely important diarrheal agent, year-long survey of retail oysters from
last six to seven days and is usually ac- responsible for 50–70% of enteritis cas- various locations in North America,
companied by vomiting. Milder forms es (Sakazaki and Balows, 1981). Al- 78% of samples from the North Atlantic,
of diarrhea due to V. cholerae O1, lasting though outbreaks caused by V. para- Pacific, and Canadian coasts contained
one to five days (usually less than three), haemolyticus do occur worldwide, they less than 0.2 MPN/g of V. vulnificus; fre-
are more difficult to distinguish from were uncommon in the United States quency and levels of V. parahaemolyticus
other mild diarrheas (Farmer et al., until four outbreaks involving more were higher. The highest levels of Vibrio
1985). than 700 people occurred in 1997– were in the Gulf Coast (Cook et al.,
V. cholerae non-O1 can cause a less 1998. This prompted the FDA to begin 2002). Some Vibrio species may be ubiq-
severe cholera-like illness, but it also a risk assessment of the public health uitous in the estuarian environment;
causes a much wider spectrum of dis- impact of V. parahaemolyticus in raw however, in many cases the presence of
eases (Morris et al., 1981), including ex- oysters, the food with which they are Vibrio is due to contamination of water
traintestinal infections (Hughes et al., most often associated (FDA/CFSAN, by sewage.
1978). While cholera and gastroenteritis 2001). A level up to 10,000 viable V. Asiatic cholera, caused by V. cholerae
caused by V. cholerae O1 is rare in the parahaemolyticus cells/g was considered O1, remains endemic to the Asian conti-
United States, illnesses caused by the acceptable until outbreaks showed that nent, and it is suspected that it was rein-
non-O1 serogroup are common and di- some oysters contained as few as 100 troduced to the United States in 1973,
arrhea usually occurs 48 hr after inges- cells/g (FDA/CFSAN, 2001). The FDA when the first case of cholera since 1911


was reported. Latin America recently ex- oysters harvested in different places— cus by 60% in 2007 compared to the av-
perienced an epidemic affecting nearly one in Louisiana and two from two dif- erage level of illness in 1995–1999 in
one million people and causing more ferent harvesters in Texas. All three had Louisiana, Texas, Florida, and California
than 9,000 deaths (Guthmann, 1995). underlying liver diseases. (NSSP, 2002).
There have been occasional outbreaks of Vibrios in general will survive at The number of vibrios in estuarine
cholera in the United States, suggesting temperatures below 10°C (50°F), but waters tends to increase as the ambient
that the microorganism has become en- their reproduction is slowed or arrested water temperature rises, resulting in
demic on the U.S. Gulf Coast, with spo- at these lower temperatures. An excep- their appearance in larger numbers in
radic cases expected to occasionally oc- tion is V. parahaemolyticus, which dies shellfish and other fishes in these waters
cur. Between 1965 and 1991, there were under refrigeration temperatures of 0– during the warmer months of the year
136 cases of cholera reported to the 5°C (ICMSF, 1996). At elevated temper- (Cook et al., 2002). This may explain the
CDC, of which 93 were acquired in the atures, the growth of vibrios in contam- increase in V. vulnificus infections in
United States. Fifty-six of the 93 cases inated seafood is extremely rapid. Gen- Florida between May and October com-
were attributed to V. cholerae O1. Con- eration times of 12–18 min are common pared to the rest of the year (CDC,
taminated crabs and other shellfish har- in various seafood held at 30–37°C (86– 1993). Special precautions should be
vested near the Gulf Coast were the 98.6°F). All of the vibrios are sensitive to taken during these months. The Model
main source of infection (Weber et al., drying, yet are able to grow in a wide Ordinance identifies specific control
1994). Large outbreaks of illness have range of sodium chloride levels, varying measures for harvesting areas where two
been eliminated by the establishment of from 0.5 to 10% with optimal growth at or more cases of V. vulnificus have oc-
adequate sewage treatment facilities. 2.2% (FDA/CFSAN, 2001). curred. In those areas, the time between
However, in 1997 more than 90,000 harvesting and refrigeration is halved,
Rwandan refugees became infected with Control Measures from 20 hr to 10 hr, in the summer
V. cholerae O1 (Anonymous, 1998). The distribution of V. cholerae and V. months. Cooling immediately upon
V. parahaemolyticus and, because of parahaemolyticus in the environment is harvesting and maintaining lower tem-
their physiological similarities, the other better understood than that of the other peratures until consumption controls
vibrios, are found mainly in marine en- human pathogenic members of the ge- the growth of vibrios in raw seafood.
vironments throughout the world. nus. This is mainly due to the lack of According to the 2001 Risk Assessment
However, in a few instances, these vibri- suitable enrichment and primary isola- conducted by FDA/CFSAN, the annual
os have been isolated from fresh-water tion media for the other vibrios, as well number of illnesses due to V. para-
or non-marine fish. In these cases, it is as their recent discovery and association haemolyticus in raw oysters could be re-
assumed that the sodium chloride con- with human illness. These vibrios are, duced from 3,000 to 240, if rapid cool-
tent of the water was elevated, or the however, thought to be distributed simi- ing was employed, or to 15, if oysters
vibrios were present because of pollu- lar to V. parahaemolyticus because of were frozen (FDA/CFSAN, 2001). Heat-
tion of the waters. A correlation be- their salt tolerance and similar physio- ing rapidly (5 min, 50°C) kills 4.5–6 logs
tween the isolation of these vibrios and logical makeup. of all vibrios. The risk assessment esti-
water temperatures also exists. Vibrios Presence in estuarine waters does not mated that there would be less than 10
are isolated more frequently and in correlate with fecal coliform counts; cases of V. parahaemolyticus infection
higher numbers during the warmer therefore, presence of the bacteria is nei- caused by raw oysters if mild heating
months of the year. Oysters from states ther restricted to nor related to poor- was used (FDA/CFSAN, 2001). Ade-
along the West Coast and British Co- quality oyster beds. There is less infor- quate cooking and avoidance of recon-
lumbia contaminated with V. para- mation concerning the occurrence of V. tamination will ensure the safety of sea-
haemolyticus caused an outbreak in mimicus in the environment and sewage. food.
North America in 1997, resulting in 209 It has been suggested, however, that this All of the disease-causing vibrios are
cases (FDA/CFSAN, 2003b). In 1998, V. microorganism may also be a normal naturally occurring in the marine envi-
parahaemolyticus in oysters and clams part of the marine estuarine environ- ronment and are thus naturally occur-
harvested from the Long Island Sound ment and may also increase in numbers ring contaminants of seafood, making it
caused an outbreak in Connecticut, during the warmer months. Vibrio may impossible to prevent the contamina-
New Jersey, and New York, and a sepa- be distributed throughout different tion of these fresh products. The most
rate outbreak occurred in the Gulf parts of the world through ballast water. important control measures to prevent
Coast. The implicated serotype (O3:K6) The Interstate Shellfish Sanitation human infections with these microor-
was recognized as pathogenic in Asia, Conference created a Model Ordinance, ganisms are hygienic measures designed
but had not previously been isolated in contained in the Guide for the Control to prevent their multiplication in these
the United States. (FDA/CFSAN, 2001). of Molluscan Shellfish, through the Na- uncooked foods and prevent the recon-
V. vulnificus is ubiquitous in coastal tional Shellfish Sanitation Program. The tamination of cooked seafood. Certain
waters from Florida to Maine. CDC re- document provides the standards for individuals (e.g., those with diabetes,
ports that between 1988 and 1995, 302 harvesting areas and specifies testing those on immunosuppressive drugs, al-
cases of V. vulnificus infections were re- methods for the waters. Because the sea- coholics, and cirrhotics) should avoid
ported in the Gulf Coast states (CDC, food industry has been required to im- the consumption of any raw seafood at
1996b). An outbreak affecting 16 indi- plement HACCP since 1997, the Model any time of the year. As long as individ-
viduals in Los Angeles was associated Ordinance also gives details on HACCP uals continue to consume raw or under-
with the consumption of raw oysters. for shellfish. The ultimate public health cooked seafood, there will continue to
The three case fatalities consumed raw goal is to reduce illness due to V. vulnifi- be Vibrio infections in the United States.


Scientific Status Summary
Staphylococcus aureus enterotoxin A indicate that less than 1µg along with Salmonella infantis, was iso-
Originally authored by Rosetta L. of toxin can result in illness (Tatini et lated from turkey that caused a food-
Newsome. Reviewed by Cynthia M. al., 1984). borne outbreak at a Florida prison in
Stewart. 1990 (Meehan et al., 1992). Methicillin-
Association with Foods resistant S. aureus (MRSA), commonly
Given adequate time, temperature, S. aureus is commonly found in the associated with hospital infections,
pH, water activity (aw), and atmosphere nose and throat (and thus on the hands caused a foodborne outbreak when a
for growth, contaminating S. aureus and fingertips) and on the hair and skin delicatessen employee prepared cole-
may multiply, and many strains may of more than 50% of healthy individuals slaw. Tests concluded that the employee
produce enterotoxins when the popula- (Bergdoll, 1979). Any food which re- carried the outbreak strain of MRSA,
tion exceeds 105 cells/g. Ingestion of the quires handling in preparation may which was presumably transferred from
thermostable enterotoxins, rather than therefore easily become contaminated. a nursing home that the employee fre-
the bacterium itself, is responsible for Infected wounds, lesions, and boils of quently visited (Jones et al., 2002).
foodborne illness. food handlers may also be sources of Although the acidity (low pH) of
contamination, as well as coughing and mayonnaise is inhibitory to the growth
Significance as a Pathogen sneezing by individuals with respiratory of staphylococci, growth may occur in
Staphylococcal food intoxication is infections. S. aureus also commonly oc- salads (such as egg or chicken), where
estimated to cause 185,000 cases of curs on the skin and hides of animals, the otherwise low pH of the mayonnaise
foodborne illness annually (Mead et al., and may thus contaminate foods from is raised or buffered by other salad in-
1999). The true incidence is unknown these animals as a result of cross-con- gredients. Food systems that contain salt
for several reasons, including poor re- tamination during slaughter. or sugar also provide a favorable envi-
sponse by victims to interviews con- A variety of foods can support the ronment for growth of S. aureus, be-
ducted by health officials; misdiagnosis growth of S. aureus. Foods which sup- cause growth of more sensitive microor-
due to symptoms being similar to those port growth best include proteinaceous ganisms is inhibited, but growth of S.
of other types of food poisoning (such foods, such as meat and meat products, aureus is not. Staphylococci can tolerate
as the vomiting caused by Bacillus cereus poultry, fish and fish products, milk and up to 10–20% salt and 50–60% sucrose.
emetic toxin); inadequate collection of dairy products, cream sauces, salads S. aureus is also tolerant to nitrite and
samples for laboratory analysis; and im- (ham, chicken, potato, etc.), puddings, may therefore multiply in curing solu-
proper laboratory examination (Ben- custards, and cream-filled bakery prod- tions or cured meats if they are subject-
nett, 1986). ucts. Staphylococci are usually outnum- ed to conditions favorable for growth.
Unlike other foodborne illnesses, bered by competitive harmless microor- S. aureus is a facultative anaerobe
which usually have longer incubation ganisms in raw foods because they do which grows best under aerobic condi-
periods, onset of staphylococcal food- not compete well with other bacteria, tions but is also capable of growth when
borne illness may occur between 30 min and it is probably for this reason that oxygen is present at reduced concentra-
and 8 hr following consumption of the raw foods are less frequently implicated tions. Some oxygen must be present,
toxin-containing food (Bergdoll, 1979). as the cause of staphylococcal food poi- however, for toxin production (Bergdoll,
Most illnesses, however, occur within 2– soning. Cooking, however, eliminates 1979; Niskanen, 1977; Tatini, 1973). The
4 hr (Bergdoll, 1979). Staphylococcal the normal competitive bacteria of raw microorganism prefers temperatures of
enterotoxins (SE) cause severe gastroen- foods; therefore, it is in prepared foods 95–98.6°F (35–37°C) but can grow at
teritis (inflammation of the intestinal such as meat, potato, and macaroni sal- temperatures as low as 44°F (67°C) or as
tract lining). Common symptoms of ads, custards, and cream-filled bakery high as 118°F (47.5°C) (Bergdoll, 1979).
staphylococcal intoxication include nau- products that growth of contaminating While heat processing and normal
sea, vomiting, retching, abdominal staphylococci may be permitted. cooking temperatures are sufficient to
cramping, sweating, chills, prostration, S. aureus intoxications are often as- kill the bacterial cells, the enterotoxins
weak pulse, shock, shallow respiration, sociated with institutions such as are heat-stable and are not inactivated
and subnormal body temperature. Re- schools and prisons where food is often by heat processing or cooking. The ab-
covery from this intoxication (which is prepared in mass quantities and held sence of viable staphylococci, therefore,
rarely fatal) usually occurs uneventfully until consumption. Lack of sanitation does not ensure that a food is safe.
within 24–48 hr. by workers and improper time-temper- Growth may occur at aw as low as
Growth of staphylococci to a popula- ature combinations can lead to contam- 0.86 under aerobic conditions or at aw
tion of a million or more cells per gram ination of the product and growth of 0.90 under anaerobic conditions. Al-
of food is considered necessary for suffi- the microorganism to levels at which though staphylococci are fermentative
cient toxin production to elicit symp- toxin is produced. Accordingly, out- and proteolytic, they do not usually
toms of food poisoning. Several anti- breaks can affect a large number of peo- produce off-odors in foods or make
genically different protein enterotoxins ple. An outbreak in 1990 in two schools them appear spoiled. Presence of the
exist (Tatini et al., 1984). To date, SE A, in Rhode Island resulted from ham pre- bacteria or their toxins in foods would,
B, C1, C2, C3, D, E, G, H, I, and J have pared at a satellite location that was sub- therefore, not be detectable by sensory
been identified (Balaban and Rasooly, sequently handled by an employee who methods.
2000). Enterotoxin A is the most toxic harbored S. aureus. The ham was stored
and the one most commonly involved in at inappropriate temperatures for at Control Measures
staphylococcal food poisoning out- least 15 hr and was not adequately re- The ubiquity of the staphylococci in
breaks. Data from outbreaks involving heated (Richards et al., 1993). S. aureus, the human and animal environment ne-


cessitates good sanitation in processing of vegetative cells. The toxicoinfection is presence of C. perfringens after cooking
operations and food handling, and strict caused by sporulation of the bacterial at 73.9°C, only two samples, both
control measures for prevention of bac- cells in the intestine, accompanied by ground pork, had levels above the detec-
terial growth and subsequent toxin pro- production of an intracellular entero- tion limit of three spores/g (Kalinowski
duction. For staphylococcal food poi- toxin. Sporulation and enterotoxin pro- et al., 2003). Nevertheless, in the United
soning to occur, four things must hap- duction may also occur in foods, how- States, from 1988 to 1997, meat and
pen: (1) the food must be contaminated ever (Craven, 1980; Naik and Duncan, poultry items were involved in at least
with enterotoxin-producing staphylo- 1977). Diarrhea and severe abdominal 33% of C. perfringens outbreaks; a
cocci; (2) the food must be capable of pain are the usual symptoms. Nausea is source was not identified nearly 20% of
supporting the growth of the contami- less common, and fever and vomiting the time, and multiple vehicles, which
nant; (3) the food must be held at a are unusual. Death is uncommon, usu- may have included meat or poultry were
temperature sufficiently high and for a ally occurring in debilitated or institu- involved in 28% of outbreaks (CDC,
sufficient period of time to permit suffi- tionalized individuals, especially the eld- 1996a; CDC, 2000b). Fish are not com-
cient growth to result in the formation erly. Illness generally lasts 24 hr, but may monly involved in outbreaks, although
of an emetic (vomiting) level of entero- last up to two weeks (FDA/CFSAN, the body surface and the alimentary ca-
toxin; and (4) the food must be con- 2003). nal of most fish of several species harbor
sumed. There is little that can be done the microorganism.
about the first two items, because most Association with Foods C. perfringens has been found, albeit
foods are subject to contamination (for C. perfringens type A can be consid- at a much lower incidence, in virtually
the reasons already given) and are capa- ered part of the microflora of soil. Vir- all types of processed foods examined.
ble of supporting growth. Control of the tually all soil samples examined have re- This is important because some of these
temperature is the most effective route vealed type A strains at levels of 103–104/ items, such as spices and herbs, are add-
to control staphylococcal food poison- ed to larger volumes of cooked foods.
ing. Indeed, the majority of staphylo- Although processed foods are rarely ve-
coccal food poisoning outbreaks occur hicles for this type of food poisoning,
because of inadequate cooling and re- Since C. perfringens will minestrone soup was the vehicle for a
frigeration of foods. Adequate heat pro- 1990 outbreak in Michigan that made
cessing and cooking and proper cooling not grow at refrigerated 32 people ill (Roach and Sienko, 1992).
and refrigeration are therefore impor-
tant control measures.
temperatures, the princi- The soup was prepared two days before
consumption and was not promptly
pal cause of virtually all cooled or adequately reheated.
Clostridium perfringens Foodservice establishments are the
Ronald G. Labbe outbreaks is failure to most likely sites for acquiring the illness.
This reflects the need for such facilities
Clostridium perfringens is probably properly refrigerate to cook large amounts of food well in
the most extensively studied anaerobic advance of serving. Because of the rela-
bacterial human pathogen. During the cooked foods, especially tively mild nature of the illness, many
last 90 years, C. perfringens has been
most closely associated with gas gan-
large portions. outbreaks, especially those involving
families, go unreported. The reported
grene. The first indication of an associa- incidence is undoubtedly only the tip of
tion with food poisoning, however, g. Types B, C, D, and E are obligate para- the iceberg. The incidence from properly
came in the 1940s from Knox and Mac- sites, mostly of domestic animals, and handled commercially prepared food is
Donald in England and McClung in the do not persist in soils. The microorgan- virtually zero.
United States (Hobbs, 1979). ism is also found in the intestinal con- Cured meat products are rarely vehi-
tents of virtually every animal exam- cles for outbreaks of C. perfringens food
Significance as a Pathogen ined, with wide variation in numbers poisoning. Two unrelated outbreaks in
Because of the degree of underre- within and between species. For exam- 1993 were due to improper holding of
porting, estimates of the number of an- ple, after chilling, carcasses were positive corned beef. The outbreaks stemmed
nual cases range from 10,000 to 250,000 for C. perfringens in 13 of 16 broiler from the fact that in both instances, the
in the United States. (FDA/CFSAN, flocks. In the affected flocks, 8–68% of corned beef was prepared in advance in
2003b; Mead et al., 1999). Strains of the individual carcasses harbored C. perfrin- mass in anticipation of the large de-
microorganism are divided into five tox- gens, with a mean of 30% (Craven et al., mand around St. Patrick’s Day. The load
in types, A to E, based on the produc- 2001). In human infants, adult levels of of C. perfringens in corned beef samples
tion of four lethal extracellular toxins C. perfringens (103–105/g) are estab- exceeded 105 CFU/g in each outbreak
(alpha, beta, epsilon, and iota). Since lished by six months of age. (CDC, 1994). In general, these products
virtually all food poisoning outbreaks Meat and poultry products are by far are considered safe when properly han-
are caused by type A strains, it is not the most common C. perfringens vehi- dled due to the curing agents them-
necessary to determine the toxin type in cles. This is not surprising, given the in- selves, the low initial spore load in such
such outbreaks. cidence of C. perfringens in such foods products, the heat treatment adminis-
Illness due to C. perfringens usually and the microorganism’s fastidious nu- tered, and the relative sensitivity to the
occurs 8–22 hr after ingestion of food trient requirements. When 197 commi- curing agents of the surviving, and per-
containing large numbers (106 or more) nuted meat samples were tested for the haps injured, spore population.


Scientific Status Summary
Control Measures poultry. Thus, preventive measures de- type G has been isolated in cases of sud-
The problem of C. perfringens food- pend to a large extent on knowledge of den and unexpected death in humans
borne illness is one associated with the proper food preparation and storage (Sonnabend et al., 1981) and infants
foodservice industry and consumers. techniques, especially temperature con- (Sonnabend et al., 1985). C. botulinum is
The two most important attributes of C. trol. In the case of C. perfringens food isolated from a variety of sources, such
perfringens are its ability to grow rapidly poisoning, it is clear that education and as soil, marine and lake sediments, feces
at elevated temperatures and its ability supervision of food handlers remain and carcasses of birds and animals, hu-
to form spores. Control measures must critical control points. man autopsy specimens, rotting vegeta-
consider both of these. tion, and foods. In addition to these
Since C. perfringens will not grow at Clostridium botulinum types, C. baratii and C. butyricum,
refrigerated temperatures, the principal Merle D. Pierson and N.R. Reddy which produce BoNT, have been isolat-
cause of virtually all outbreaks is failure ed from infant botulism cases (Hall et
to properly refrigerate cooked foods, es- The popularity of botulinum neuro- al., 1985; McCroskey et al., 1986; Suen et
pecially large portions. An analysis of toxin (BoNT), also known as “Botox,” to al., 1988).
outbreaks occurring between 1973 and reduce facial wrinkles and the potential C. botulinum produces a BoNT,
1987 showed that 97% were due to im- to use C. botulinum and its neurotoxin which is a simple polypeptide that con-
proper holding temperatures (Bean and as agents of intentional contamination sists of a 100-kDa “heavy” chain joined
Griffin, 1990). Spores on raw meat and have sparked renewed interest in this by a single disulfide bond to a 50-kDa
poultry can survive cooking and resume pathogen, historically associated with “light” chain. Three-dimensional struc-
vegetative cell growth when the cooling home-canned or prepared products. ture of type A BoNT has been resolved
product reaches a suitable temperature. The etiologic agent of botulism was first to 3.3Å resolution using data collected
Rapid, uniform cooling is therefore im- isolated from inadequately cured ham from multiple crystals at 4°C (Lacy et
perative. Prior to 1996, USDA/FSIS pre- in 1896 by E.P.M. van Ermengen. Since al., 1998). BoNTs are toxic to humans
scribed specific time-temperature com- C. botulinum spores are widely distrib- and animals; on a weight basis, they are
binations for the cooking and cooling of uted, they may find their way into pro- the most lethal substances known, being
RTE meats. In 1999, USDA issued a final cessed foods through raw food materials up to 100,000 times more toxic than
rule allowing processors some flexibility or by contamination of foods after pro- sarin (Shapiro et al., 1998). The exact le-
in determining the process. With respect cessing and cause botulism in humans. thal dose of BoNT for humans is not
to C. perfringens, any cooling operation Processors and consumers must take known. However, by extrapolation, Ar-
that prevented one log of growth would preventive measures to eliminate C. bot- non and others (2001) estimated the le-
meet the standard. The process does not ulinum or to inhibit growth and toxin thal dose of crystalline type A BoNT for
need to be validated for uncured meats production by this microorganism to humans from primate data. The lethal
cooled from 54.4°C (130°F) to 26.7°C prevent outbreaks of botulism from oc- dose of crystalline type A BoNT for a 70
(80°F) in less than 1.5 hr, and further curring. Instances of botulism resulting kg (154 lb) human would be approxi-
cooled to 4.4°C (40°F) in less than 5 hr. from improper canning are primarily mately 0.09–0.15µg via intravenous or
(Anonymous, 1999). Cooking also re- associated with home canning, not in- intramuscular injection, 0.70-0.90µg via
duces the oxidation/reduction potential dustrial processes. This results in a lim- inhalation, and 70µg via oral ingestion
and thereby promotes anaerobic condi- ited number of cases annually, but does (1µg/kg).
tions, a factor especially important in not mean that attention should be di- Type A BoNT, which causes roughly
liquid foods and rolled meats, where the verted from this pathogen. half the annual cases of foodborne bot-
contaminated outside surface is rolled ulism, is more lethal than types B and E,
into the middle. Other factors include Significance as a Pathogen which are equally responsible for the re-
preparation of food a day or more be- Seven types (A, B, C, D, E, F, and G) maining cases (Shapiro et al., 1998). The
fore serving, inadequate hot-holding, of C. botulinum are recognized based on toxin is a protein that can be inactivated
and inadequate reheating of cooked, the antigenic specificity of toxin. How- by heat (80°C for 10 min or 85°C for 5
chilled foods. Cooked foods should be ever, all types of C. botulinum produce min). The toxin in solution is colorless
divided into small portions so that re- protein neurotoxins with similar effects and odorless and can be absorbed into
frigeration temperature is reached with- on an affected host. The types of C. bot- the blood stream through the respirato-
in two hr. These foods should be re- ulinum differ in their tolerance to salt ry mucous membranes as well as
heated to a minimum internal tempera- and water activity, minimum growth through the wall of the stomach and in-
ture of 74°C (165°F) immediately before temperature, and heat resistance of testine. Type A BoNT is the first biologi-
serving to destroy vegetative cells. spores. All type A strains are proteolytic, cal toxin licensed for treatment of hu-
Cooked meat should be kept above 60°C and all type E strains are nonproteolytic. man diseases, namely for cervical torti-
(140°F) or below 4°C (40°F). Types B and F both contain some pro- collis, strabismus, and blepharospasm
It is not possible to prevent carriers teolytic and nonproteolytic strains. associated with dystonia, to reduce facial
of C. perfringens from handling food, Types A, B, E, and F are involved in hu- wrinkles and hemifacial spasm, and for
since all people harbor the microorgan- man botulism; type C causes botulism several unlicensed treatments of other
ism in their intestinal tract. Similarly, in birds, turtles, cattle, sheep, and hors- human diseases (Arnon et al., 2001;
the bacterium is present in a wide vari- es; and type D is associated with forage Johnson, 1999; Schantz and Johnson,
ety of foods. However, food handlers poisoning of cattle and sheep in Austra- 1992).
play a minimal role as a contamination lia and South Africa. No outbreaks of Botulism is currently classified into
source of C. perfringens in meat and type G have been reported; however, four categories: (1) classical foodborne


botulism and intoxication caused by the control is striking. Recommended treat- the eastern states and in Europe. Type E
ingestion of preformed BoNT in con- ment is primarily supportive care. Re- is most often associated with water envi-
taminated food; (2) wound botulism, cent clinical studies have shown that the ronments.
the rarest form of botulism, which re- use of botulism immune globulin (BIG) Since fruits and especially vegetables
sults from the elaboration of BoNT in reduces the time of hospitalization and are often in contact with soil, these
vivo after growth of C. botulinum in an the need for supportive ventilation and foods can easily become contaminated
infected wound; (3) infant botulism, in tube feeding (AAP, 2000). Antimicrobial with spores of C. botulinum. The micro-
which botulinal toxin is elaborated in therapy is not recommended (Sakagu- organism has been isolated from fresh
vivo in the intestinal tract of an infant chi, 1979). and processed meats, but the incidence
who has been colonized with C. botuli- Due to the rarity of the illness, botu- is generally low (Hauschild and Hilshe-
num; and (4) an “undetermined” classi- lism is often misdiagnosed; however, imer, 1980; Rhodehamel et al., 1992).
fication of botulism for those cases in- rapid detection is necessary for the C. botulinum spores have been de-
volving individuals older than 12 timely administration of antitoxin. De- tected in honey and corn syrup (Lynt et
months in which no food or wound tection of the toxin, either in a suspected al., 1982). C. botulinum is a natural con-
source is implicated (Anonymous, 1979; food vehicle or the serum or stool of taminant of fish. The intestinal tract of
Rhodehamel et al., 1992). suspected cases, is generally accom- fish and its contents have been reported
Foodborne botulism results from the plished using an Association of Analyti- to be the main reservoirs (Huss et al.,
consumption of food in which C. botuli- cal Communities-approved mouse bio- 1974). Since many processes do not in-
num has grown and produced toxin. assay. Amplified enzyme-linked immun- clude steps that are lethal to spores of C.
The toxin is absorbed and irreversibly osorbent assay (ELISA) and amplified botulinum, the microorganism may be
binds to peripheral nerve endings. Signs found occasionally in some finished
and symptoms of botulism develop 12– products, such as smoked fish.
72 hr after consumption of the toxin- Proteolytic types A, B, and F strains
containing food. The signs and symp-
Conditions that favor C. produce heat-resistant spores that are a
toms include nausea; vomiting; fatigue;
dizziness; headache; dryness of skin;
botulinum growth and major concern in the processing of low-
acid canned foods. The nonproteolytic
mouth; and throat; constipation; paraly- toxin production include a types B, E, and F strains produce spores
sis of muscles; double vision; and diffi- of low heat resistance and cause prob-
culty breathing. Duration of illness relatively high-moisture, lems primarily in pasteurized or un-
ranges anywhere from 1–10 days or heated foods (Sperber, 1982). Proteina-
more, depending upon the host resis- low-salt, low-acid (pH > ceous foods, such as meats, and nonpro-
tance, type and amount of toxin ingest- teinaceous foods, such as vegetables, can
ed, and type of food. Treatment includes 4.6) food that is devoid of provide sufficient nutrients for growth
administration of botulinal antitoxin and toxin production by C. botulinum.
and appropriate supportive care, partic-
oxygen and stored without The proteolytic types digest proteins in
ularly respiratory assistance lasting be-
tween two to eight weeks (Shapiro et al.,
refrigeration. foods and produce foul odors, which
may warn consumers. However, there
1998). Recovery may take several weeks have been outbreaks where only a small
to months. Death may result; however, ELISA/enzyme-linked coagulation assay amount of food having an off-odor was
the mortality rate is less than 10%. (ELCA) show promise for more rapid consumed or food without evidence of
Infant botulism, which affects infants detection of toxin; however, these assays spoilage was consumed. The latter is es-
under 14 months of age, was first recog- have not yet replaced the mouse bioas- pecially true for the nonproteolytic
nized in California in 1976 (Midura and say in general use (Ferreira, 2001; Ferrei- strains (Lynt et al., 1975).
Arnon, 1976). This type of botulism is ra et al., 2003; Roman et al., 1994). The proteolytic and nonproteolytic
thought to be caused by the ingestion of types of C. botulinum differ in their tol-
C. botulinum spores that colonize and Association with Foods erance to salt, water activity, minimum
produce toxin in the intestinal tract of Spores of C. botulinum are widely growth temperature, and spore heat re-
infants (Paton et al., 1982; Wilcke et al., distributed in cultivated and forest soils, sistance. The optimum temperature for
1980). Honey has been implicated as a shore and bottom deposits of streams, growth and toxin production by the
possible source of spores. Other non- lakes, and coastal waters; gills and vis- proteolytic types is about 35°C (95°F),
sterilized foods, as well as nonfood cera of crabs and other shellfish; and the with very slow growth at both 12.5°C
items in the infant’s environment, may intestinal tracts of fish and animals (Ey- (55°F) and 50°C (122°F); however, at
the latter temperature, toxin may be
also be sources of spores. Infant botu- les, 1986; ICMSF, 1980; Lynt et al., 1975;
slowly inactivated (Bonventre and
lism is diagnosed by demonstrating bot- NFPA/CMI, 1984; Rhodehamel et al.,
Kempe, 1959). The nonproteolytic types
ulinal toxins and spores in the infant’s 1992; Sakaguchi, 1979). Although the can grow between 3.3°C (38°F) and
stools. spores are widespread, only about 22–24 45°C (113°F), with an optimum for
Clinical symptoms of infant botu- cases of foodborne botulism are report- growth and toxin production at about
lism start with constipation that occurs ed to the CDC annually (Shapiro et al., 30°C (86°F). Refrigeration above 3.3°C
after a period of normal development. 1998; Townes et al., 1996). Type A oc- may not be a complete safeguard against
This is followed by poor feeding, lethar- curs more frequently in soils of the botulism for foods containing nonpro-
gy, weakness, pooled oral secretions, western regions of the United States, teolytic strains (Eklund et al., 1967; Pa-
and weak or altered cry. Loss of head and type B is found more frequently in tel et al., 1978).


Scientific Status Summary
Almost every type of food product linum spores or control growth and control measures, such as proper refrig-
(dairy products, vegetables, jarred pea- subsequent toxin production. Reviews eration and frozen storage, must be
nuts, fishery products, meat products of specific treatments and hurdle con- maintained from purchase until con-
[beef, pork, and poultry], and condi- cepts used for control of C. botulinum sumption. If a commercial product is
ments [chili sauce, chili peppers, tomato in a variety of food products have been mishandled, control measures are com-
relish, and salad dressing]) has been im- published (Hauschild, 1989; Rhode- promised and botulism may result.
plicated in foodborne botulism out- hamel et al., 1992).
breaks (Arnon et al., 2001; Aureli et al., Typical methods used to prevent Bacillus cereus
2000; Chou et al., 1988; Kalluri et al., botulism include reduction of vegetative Michael P. Doyle
2003; Peck, 2002; Rhodehamel et al., cell and/or spore contamination in the
1992; Weber et al., 1993). The largest food by heat treatment (e.g., pressure Bacillus cereus has been a recognized
U.S. outbreak since 1978 occurred in cooking for canning) to obtain “com- cause of foodborne illness for almost 50
1994 as the result of improper storage of mercial sterility” and use of lower heat years. Two types of illnesses, the emetic
baked potatoes later used to make dip. treatments (pasteurization) in combina- and diarrheal responses, are caused by
Of the 30 reported cases, four required tion with other control measures. Ni- two distinct enterotoxins produced by
mechanical ventilation (Angulo et al., trite and salt (in a brine solution) are this microorganism (Melling et al.,
1998). Cheese and other dairy products control measures used in addition to 1976).
were implicated in less than 1% of re- heat treatment for low-acid canned
ported cases of C. botulinum intoxica- meats (e.g., canned ham). In addition to Significance as a Pathogen
tion since 1899 (Townes et al., 1996). these controls, refrigeration is an impor- An estimated 27,000 cases of food-
Improper handling and storage of com- tant control for perishable vacuum- borne illness due to B. cereus occur an-
mercially canned cheese was responsible packaged meats. Acidification is used for nually in the United States (Mead et al.,
for a restaurant outbreak in 1993 affect- other food products such as pickles, 1999). A large molecular weight protein
ing eight people and resulting in one mayonnaise, and canned fruit products. causes the diarrheal response, whereas
death (Townes et al., 1996). In 1989, Reduction of moisture level (drying) be- cereulide, a small peptide stable for 20
toxin production in garlic-in-oil caused low an aw of 0.93 is employed in certain min at 121°C, causes the emetic re-
three cases of botulism. Since this was foods. Frozen storage is yet another sig- sponse (Granum, 1997). The diarrheal
not the first time this type of product, nificant factor in controlling pathogen response, which closely mimics symp-
which had a pH >4.6, was implicated, growth and subsequent toxin formation. toms of the illness caused by C. perfrin-
FDA began requiring that products of The excellent safety record of cured gens, generally produces mild symptoms
this nature be acidified or contain anti- meats relative to botulism outbreaks has that usually develop between 6–15 hr
microbial agents (Morse et al., 1990). been largely attributed to the use of ni- after ingestion. The emetic (or vomit-
FDA issued guidance for labeling of trite as a curing ingredient. Many stud- ing) response occurs within a few (one
foods requiring refrigeration following ies have been published on the efficacy to six) hr after ingestion, closely mim-
botulism outbreaks caused by black of sodium nitrite in inhibiting C. botuli- icking symptoms produced by staphylo-
bean dip and clam chowder. Illness num growth and toxin production in coccal enterotoxin. Symptoms of the di-
could have been prevented had the perishable cured meats such as wieners, arrheal syndrome include diarrhea, ab-
items, which were not commercially bacon, canned ham, luncheon meat, and dominal cramps, and tenesmus, whereas
sterile, been properly refrigerated by the canned comminuted meat (Rhode- nausea and vomiting are the principal
consumer. Although the products were hamel et al., 1992). In perishable cured symptoms of the emetic syndrome. Re-
displayed in the refrigerated section of meats, safety cannot be totally attribut- covery is usually complete within 24 hr
the grocery store, FDA felt that because ed to nitrite alone, but a variety of fac- after onset, and further complications
of the packaging consumers did not fol- tors and their interaction with nitrite do not occur. The diarrheal syndrome
low the directions for refrigeration. provide protection against botulinal results following ingestion of large
Temperature abuse allowed the growth growth and toxin production. Factors numbers of the microorganism, whereas
of C. botulinum to toxin-producing lev- such as heat treatment, acidity (pH), the emetic syndrome is likely to result
els. To prevent future outbreaks, FDA salt, and bacterial spore level influence from ingestion of preformed toxin in
recommended that foods that may the effect of nitrite on C. botulinum the food.
present a safety risk if not refrigerated growth and toxin production. Other
bear the label, “IMPORTANT: Must Be curing adjuncts, such as ascorbic acid Association with Foods
Kept Refrigerated” (FDA, 1997). and sodium erythorbate, may also influ- B. cereus is common in soil and on
ence the efficacy of nitrite. vegetation and can be readily isolated
Control Measures The greater incidence of botulism from a variety of foods, including dairy
Conditions that favor C. botulinum due to improper home processing and products, meats, spices and dried prod-
growth and toxin production include a storage of foods, particularly home- ucts, and cereals (especially rice). In
relatively high-moisture, low-salt, low- canned foods, compared to commercial- view of its wide distribution in the envi-
acid (pH > 4.6) food that is devoid of ly processed foods reflects the food in- ronment, B. cereus is ingested from time
oxygen and stored without refrigeration dustry’s greater awareness and control to time and inevitably is part of the
(above 38°F or 3.3°C). The food indus- of the key factors in inhibition of C. bot- transitory human intestinal microflora.
try uses a variety of physical and chemi- ulinum growth and toxin production. Studies have revealed that low numbers
cal treatments to either destroy C. botu- Consumers must recognize that certain of B. cereus are present in the intestinal


tract of more than 10% of the healthy quantities will facilitate rapid cooling. 30% to 80% despite antibiotic treatment
adult population (Ghosh, 1978; Shina- Ideally, foods should be cooled to below (Muytjens et al., 1983). There have been
gawa et al., 1980). 15°C (59°F) within two to three hr after conflicting reports regarding low birth
Foods that have been implicated as cooking. Regarding preparation of rice weight as a risk factor for infection
vehicles in outbreaks of B. cereus diar- and fried rice, the following recommen- (FDA/CFSAN, 2002; Muytjens et al.,
rheal-type food poisoning include cere- dations have been made: (1) prepare 1983; van Acker, 2001); however, the
al dishes that contain corn and corn quantities of rice as needed; (2) keep Contaminants and Natural Toxicants
starch, mashed potatoes, vegetables, prepared rice hot (55–63°C, 131–146°F); Subcommittee of the FDA/CFSAN’s
meat products, puddings, soups, and (3) cool cooked rice quickly; and (4) re- Food Advisory Committee reviewed risk
sauces. B. cereus emetic-type food poi- heat cooked rice thoroughly before serv- factors for E. sakazakii infections and
soning is most frequently associated ing (Bryan et al., 1981; Gilbert et al., concluded that infants born at less than
with fried or boiled rice dishes 1974; Moreland, 1976; PHLS, 1976; Sly 36 weeks gestational age were at risk un-
(Johnson, 1984). Chicken fried rice was and Ross, 1982). til six weeks post-term. Other risk fac-
implicated in a 1993 outbreak in Virgin- B. cereus spores in foods can be de- tors identified were hospitalization in
ia that affected 14 people (FDA/CFSAN, stroyed by retorting (pressure cooking) level-two or level-three neonatal inten-
2003b). Other starchy foods such as or applying an equivalent thermal pro- sive care units and immunocompro-
macaroni and cheese also have been in- cess or by irradiation. However, such mised health status (FDA/CFSAN,
criminated as vehicles of the emetic syn- treatments may be too severe and, 2003a).
drome. hence, unacceptable for many foods. Illness symptoms normally appear a
B. cereus is a spore-forming microor- few days after birth, and the health of
ganism whose spores will generally sur- Enterobacter sakazakii the infant rapidly deteriorates
vive cooking. Spores of the microorgan- Jennifer C. McEntire and Francis F. (Muytjens et al., 1983). Infection may
ism normally occur on many foods Busta. Reviewed by R. Bruce result in meningitis (58%), necrotizing
from harvest through primary process- Tompkin enterocolitis (29%), or sepsis (17%). In
ing. The microorganism is not consid- one outbreak in which 11 infants were
ered a hazard at the very low levels typi- Advances in medicine have vastly im- positive for E. sakazakii, one developed
cally present in food. However, prob- proved the mortality rate for infants. meningitis and four others had clinical
lems develop when food (especially Unfortunately, this population is partic- signs of severe sepsis, although the mi-
cooked foods which are devoid of most ularly susceptible to often-fatal infection croorganism could not be isolated from
heat-sensitive microbial competitors) is by Enterobacter sakazakii, introduced the blood (Arseni et al., 1987). Bactere-
held at 10–55°C (50–131°F) for a long through reconstituted powdered infant mia is often, but not necessarily, con-
period of time. Under these conditions, formula. firmed (Muytjens et al., 1983).
the microorganism grows to large num- The severe consequences of infection
bers, releasing toxin during growth in Significance as a Pathogen in some cases may be linked to the pro-
the food and in the intestinal tract fol- As of 1989, 20 cases of neonatal in- duction of enterotoxin by E. sakazakii.
lowing ingestion. Although ingestion of fection by E. sakazakii were reported More than 20% of the 18 tested strains
more than 105 cells/g is required to pro- worldwide (Biering et al., 1989). By produced enterotoxin. High levels (108
duce illness (Hobbs and Gilbert, 1974), 2003, 48 neonatal cases were recognized cfu) of each strain were lethal to mice
ingesting large numbers of B. cereus (FDA/CFSAN, 2003b). Within the last when administered by intraperitoneal
does not always produce illness (Dack et several years, awareness of the problem injection. Peroral administration of the
al., 1954). To date, all outbreaks of both associated with this pathogen has in- same levels were only lethal for two
types of B. cereus illness have resulted creased; as a result, research and reports strains (Pagotto et al., 2003).
because of improper holding tempera- of E. sakazakii infection in infants have When infection does not result in
tures or slow cooling of large amounts also risen. death, the affected infant may have per-
of food. Because these illnesses are in- In 1980, yellow-pigmented Entero- manent neurological or developmental
toxications, they are not infections and bacter cloacae was recognized as its own deficiencies. In one case, mortality was
are not transmitted. It does not appear species—E. sakazakii. Although infec- averted by months of antibiotic treat-
that processing of raw agricultural com- tion by this microorganism has been re- ment, but the patient was mentally re-
modities contributes to the incidence of ported since the 1960s, the pathogen tarded and paralyzed by age two (Bier-
B. cereus illness. was not recognized as a cause of food- ing et al., 1989). In another study of
borne illness because the ecology of the eight infected infants, the two survivors
Control Measures microorganism was unknown. were both retarded, suffered from hy-
Measures to reduce or eliminate B. Infection by E. sakazakii is an ex- drocephalus, and eventually died
cereus food poisoning are well estab- tremely rare event. Six of the 58 report- (Muytjens et al., 1983). However, full re-
lished. Most disease incidents result ed cases of E. sakazakii infection world- covery is also possible (Simmons et al.,
from time-temperature abuse of food in wide involved individuals more than 1989).
food-handling establishments. This can four years of age, and the median age Infants may be colonized with E.
be prevented by holding foods at greater was 74 (FDA/CFSAN, 2003b). The vast sakazakii without developing symptoms
than 60°C (140°F) until served, or rap- majority (83%) of cases have been re- (Arseni et al., 1987; FDA/CFSAN, 2002).
idly cooling foods to below 10°C (50°F) ported in infants less than one year of Although colonization and fecal car-
for storage. Refrigerating foods in small age, where the fatality rate ranged from riage may last 8–18 weeks, secondary


Scientific Status Summary
transfer is not known to occur (Arseni similar regardless of whether the formu- of commercially sterile liquid formula in
et al., 1987; Block et al., 2002). la was manufactured through wet-mix- lieu of powdered infant formula for at-
ing, spray drying, or dry blending, or if risk infants. The FDA/CFSAN Advisory
Association with foods the formula was made with milk or soy Committee subcommittee (2003a)
Although powdered infant formula (FDA/CFSAN, 2004). A survey of pow- charged with determining if there was a
was postulated as the vehicle for E. saka- dered infant formula from 35 countries link between E. sakazakii infection and
zakii infection as early as 1983 showed that more than 14% of samples powdered infant formula reiterated this
(Muytjens et al., 1983), the first conclu- were positive for E. sakazakii. This in- recommendation.
sive evidence linking the infectious cluded two of 12 samples from pow- To decrease the risk of infant infec-
microorganism with the product was in dered infant formula purchased in the tion by E. sakazakii, FDA prepared guid-
1989 (Biering et al., 1989). After several United States. The levels of E. sakazakii ance for the preparation and use of
cases of infant infection in Iceland, tests were low—0.36 and 0.92 cfu/100 g powdered infant formula in neonatal
of the powdered milk showed that the (Muytjens et al., 1988). Levels of the units (FDA/CFSAN, 2002). Time and
microorganism could be isolated from pathogen were less than 1 cfu/100 g in temperature control are key. Initially,
all lot numbers examined. However, nei- 17 of 20 positive samples, and all tested guidance proposed using boiling water
ther every individual sample nor every to reconstitute the powder and destroy
package from a lot showed E. sakazakii the microorganism, but essential nutri-
contamination after enrichment, indi- ents could potentially be destroyed as
cating that the microorganism was Although E. sakazakii well. The thermotolerance of the
present at low levels. Plasmid analysis microorganism seems to be strain-de-
and antibiograms of 22 out of 23 strains contamination of pow- pendent with the more tolerant strains
isolated from the formula were identical having D58°C values up to 600 sec (Edel-
to the strains that caused illness (Biering dered infant formula son-Mammel and Buchanan, 2004).
et al., 1989). These techniques, as well as While pasteurization should be suffi-
chromosomal restriction endonuclease occurs at very low levels, cient to kill the pathogen, the microor-
analysis, ribotyping, arbitrarily primed
PCR, and multilocus enzyme electro-
generally less than 1 cfu/ ganism may be more heat resistant than
other Enterobacteriaceae (Breeuwer et
phoresis, have been used to conclusively 100 g, some infants with al., 2003; Nazarowec-White and Farber,
link outbreak strains with strains isolat- 1997). Edelson-Mammel and Buchanan
ed from formula in several other out- the associated risk fac- (2004) showed that preparing formula
breaks (Clark et al., 1990; Simmons et with hot, but not boiling, water (i.e.,
al., 1989; van Acker et al., 2001). tors are susceptible to 70°C) is sufficient to reduce E. sakazakii
After a fatal case of E. sakazakii infec- by more than 3.9 logs within about 15
tion was confirmed in a premature in- infection. sec. Although changes in preparation
fant in Tennessee, 49 other infants in the and storage of formula may help pre-
hospital were screened for infection or vent infections, guidance and recom-
colonization over a 10-day period. The samples complied with Codex Alimen- mendations do not address reducing
microorganism colonized in seven as- tarius recommendations for coliform contamination at the production level.
ymptomatic infants and caused either counts. The Codex standard requires The survival of E. sakazakii in pow-
confirmed or suspected infection in four of five samples to have no positive dered infant formula may be partially
three others. Pulsed-field gel electro- tubes for coliforms in a three-tube due to the ability of the microorganism
phoresis confirmed that the strain of E. MPN; the fifth sample may contain up to survive desiccation. Breeuwer et al.
sakazakii isolated from the cerebral spi- to 20 cfu/g (FAO, 1994). The batch of (2003) speculated that this is related to
nal fluid of an infected infant was iden- powdered infant formula implicated in trehalose accumulation in stationary
tical to the strain cultured from opened a Belgian outbreak also met the specifi- phase cells. Although the microorgan-
and unopened packages of infant for- cations of Codex Alimentarius, but not ism presumably does not survive pas-
mula (FDA/CFSAN, 2002). As a result, the more stringent Belgian law which teurization, it may be able to survive the
the implicated lot was recalled. A sepa- requires all samples to have less than 1 conditions of powdered milk if intro-
rate, unrelated recall of powdered infant cfu/g. Levels of E. sakazakii were so low duced during or after drying. This is
formula produced by a different manu- that the microorganism was not initially consistent with Muytjens et al. (1988),
facturer was conducted in 2003, again detected in the dry powder, and its con- who speculated that the low levels of the
due to the presence of E. sakazakii. tinued use resulted in another case (van pathogen indicate that E. sakazakii is in-
A 2002 FDA field survey collected 22 Acker et al., 2001). troduced through post-process contam-
samples of finished infant formula from ination.
eight different plants. Five samples Control measures An understanding of the environ-
(22.7%) were positive for E. sakazakii at Although E. sakazakii contamination mental reservoir(s) would facilitate con-
the lowest detectible level, 0.36 MPN/ of powdered infant formula occurs at trol of the pathogen. Until recently, this
100 g. The positive samples included very low levels, generally less than 1 cfu/ was unknown. Insects recently have
four out of 14 formulas for full-term in- 100 g, some infants with the associated been suggested as carriers of E. sakaza-
fants and one of four made specifically risk factors are susceptible to infection. kii. For example, Mexican fruit flies were
for pre-term infants. The study showed The current control measure used by shown to harbor the microorganism
that the percent of positive samples was hospitals to prevent infection is the use (Kuzina et al., 2001). Hamilton et al.


(2003) reported the isolation of E. saka- though one report isolated E. sakazakii baked potato. J. Infect. Dis. 178(1): 172-177.
zakii from the larvae of Stomoxys calci- from powdered milk, the cause of infec- Anonymous. 1979. Botulism in the United States, 1899-
1977. Handbook for Epidemiologists, Clinicians, and
trans, commonly known as the stable fly. tion in neonates was largely unknown. Laboratory Workers. Centers for Disease Control and
Rats also have been identified as a Strides have since been made to im- Prevention, Atlanta, Ga.
source of the pathogen (Gakuya et al., prove food safety, and fortunately, some Anonymous. 1986. Salmonellosis outbreak, Final Task
2001). These reports stress the impor- of the pathogens discussed are currently Force Report, Sept. 13, 1985. Hillfarm Dairy, Melrose
recognized as minimal contributors to Park, Ill.
tance of appropriate pest control as a Anonymous. 1998. Cholera outbreak among Rwandan
means to reduce the presence of E. saka- foodborne illness. The emergence of refugees–Democratic Republic of Congo, April, 1997.
zakii in production facilities. The pres- new pathogens continues, not unex- Morb. Mortal. Weekly Rep. 47(19): 389-391.
ence of the microorganism in five of 16 pectedly, as the cause of foodborne ill-
homes and eight of nine manufacturing ness is unknown in 81% of cases (Mead 00052860.htm, accessed 11/24/03.
Anonymous. 1999. Performance standards for the pro-
facilities producing a variety of dried et al., 1999). This Scientific Status Sum- duction of certain meat and poultry products. Fed. Reg.
foods suggests this opportunistic patho- mary has focused on the bacteria of sig- 64(3): 732-749.
gen is more ubiquitous than had been nificance in foodborne disease. The Arnon, S.S., Schechter, R., Inglesby, T.V., Henderson,
previously assumed, making control pathogenic (disease-causing) bacteria D.A., Barlett, J.G., Ascher, M.S., Eitzen, E., Fine, A.D.,
discussed in this summary cause most Hauer, J., Layton, M., Lillibridge, S., Osterholm, M.T.,
more difficult (Kandhai et al., 2004). O’Toole, T., Parker, G., Perl, T.M., Russell, P.K., Swerd-
The FDA/CFSAN Advisory Commit- of the known bacterial foodborne ill- low, D.L., and Tonat, K. 2001. Botulinum toxin as a bi-
tee subcommittee (2003a) encouraged ness in North America. Certain charac- ological weapon. JAMA. 285(8): 1059-1070.
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