Clostridium perfringens
R Labbe, University of Massachusetts, Amherst, MA, USA
V Juneja, Agricultural Research Service, Wyndmoor, PA, USA
r 2014 Elsevier Ltd. All rights reserved.
This article is a revision of the previous edition article by DM Broda,
JA Boerema, volume 2, pp 793–798, © 2004, Elsevier Ltd.
Glossary
Enterotoxin A toxin produced in the intestine.
Gastroenteritis The inflammation of stomach or intestine.
Plasmid A genetic element separate from the nucleus and
which is not required for growth. The genes carried in
plasmids provide antibiotic resistance or mediate toxin
formation.
Introduction
Clostridium perfringens is an opportunistic pathogen capable of
causing a broad spectrum of human and veterinary disease
conditions, including gas gangrene, meningitis, appendicitis,
respiratory and urinary tract infections, septicemia, sudden
infant death syndrome, and a variety of gastrointestinal dis-
orders. The association of this microorganism with outbreaks
of food poisoning has been known since the turn of the
nineteenth century, but its etiological role as a causative agent
of human foodborne disease was not established until the
1940s. Today, C. perfringens is recognized as a principal
causative agent of two forms of foodborne disease: C. per-
fringens type A gastroenteritis and C. perfringens type C necrotic
enteritis. The symptoms of the gastroenteritis are usually mild
and rarely fatal; however, owing to its high incidence this
condition is a substantial public health concern. The necrotic
enteritis, also known as pigbel or darmbrand, is a severe dis-
ease with a mortality rate of up to 25%, but it is exceptionally
rare in Western countries. Consequently, the emphasis in this
article will be on C. perfringens type A gastroenteritis and its
causative agent(s).
Characteristics of C. Perfringens
Clostridium perfringens is a Gram-positive, spore-forming, en-
capsulated microorganism.
Vegetative cells of C. perfringens are straight rods with blunt
ends, occurring singly or in pairs. Spores are large and oval,
distending the cell at either the central or subterminal pos-
ition. Spores are rarely observed in foods and/or in laboratory
cultures.
Clostridium perfringens is proteolytic and saccharolytic. The
majority of C. perfringens strains reduce sulfite to sulfide,
hydrolyze gelatin, reduce nitrate to nitrite, produce acid from
lactose, are lecithinase-positive and ferment sucrose. In contrast
to other sulfite-reducing anaerobes, C. perfringens is nonmotile.
Clostridium perfringens grows optimally at temperatures
between 43 and 47 °C, and at these temperatures it has a
Encyclopedia of Meat Sciences, Volume 2 doi:10.1016/B978-0-12-384731-7.00037-4
Polymerase chain reaction (PCR) A laboratory method of
amplifying specific gene(s) that may be involved in
virulence by certain bacteria.
Spore A dormant structure produced by bacteria which is
usually resistant to physical agents such as heat.
generation time of less than 10 min. Typically, the growth
range is from 15 to 50 °C. Vegetative cells of C. perfringens are
sensitive to low temperatures, such as those employed for re-
frigerated storage of foods. Generally, C. perfringens cells are
sensitive to heat and in laboratory media are easily destroyed
by exposure to temperatures above 55 °C. However, the sen-
sitivity of vegetative cells to heat is thought to be strain spe-
cific. Spores of C. perfringens are relatively cold resistant and
can survive refrigeration or freezing at −18 °C. C. perfringens
spores are renowned for their high resistance to heat, with
D95 °C values (the time in minutes at 95 °C required for a 90%
reduction in a population of viable spores) exceeding 200 min
in meat-based media. Heat resistance of C. perfringens spores
varies depending on both genetic and environmental factors.
Reports indicate that strains implicated in C. perfringens type A
gastroenteritis outbreaks may show D95 °C values 60 times
higher than those obtained for nonoutbreak strains. This re-
flects the location of the cpe gene on the chromosome or on a
plasmid (see section Molecular Methods).
Clostridium perfringens grows optimally at pH values be-
tween 6.0 and 7.0, and its growth is inhibited at pH values
below 5 and above 8.3. The minimum water activity (aw) that
will permit growth of C. perfringens is between 0.93 and 0.97.
The organism is relatively tolerant to oxygen but will not
produce colonies on the surface of solid media exposed to air.
Under carbon dioxide atmospheres, the growth of C. perfrin-
gens cells is somewhat inhibited but not completely prevented.
Growth is completely inhibited by either 6–8% NaCl,
10 000 ppm NaNO3, or 400 ppm NaNO2. However, when
these salts are used together, the inhibition of growth occurs
with substantially lower concentration of each salt.
Clostridium perfringens produces a variety of toxins that are
detrimental to humans and animals. Of the greatest signifi-
cance to food-borne disease is C. perfringens enterotoxin (CPE),
which belongs to a group of endotoxin that are produced in-
side the bacterial cell. CPE is a polypeptide of 319 amino acids
and has a molecular weight of approximately 35 kDa. It is a
unique protein that has only limited amino acid sequence
homology with other bacterial proteins. CPE is sensitive to
heat, and it is readily inactivated by 5 min exposure to a
335
336 Microbiological Safety of Meat | Clostridium perfringens
temperature of 60 °C. In contrast to vegetative cells of C. per-
fringens, CPE retains its biological activity during refrigerated
storage. Intracellular synthesis of CPE occurs throughout
the various growth stages of the bacterium but increases ex-
ponentially (at least 1500-fold) during sporulation. CPE
accumulates in the cytoplasm of the sporulating cell and is
released only when C. perfringens cells lyse to free mature
spores.
In addition to CPE, the organism produces at least 15
extracellular toxins or exotoxins, with novel C. perfringens
toxins continuing to be discovered. Exotoxins are thought not
to be responsible for the symptoms of gastroenteritis, but β1
and β2 toxins induce hemorrhagic necrosis of the intestinal
mucosa, which is characteristic of food-borne necrotic enter-
itis. On the basis of mouse lethality tests and according to the
various combinations of four major exotoxins (alpha, beta,
epsilon, and iota), C. perfringens is divided into five tox-
inotypes, A–E. Each toxinotype causes distinct disease symp-
toms, with C. perfringens type A being associated with either
gas gangrene or gastroenteritis symptoms, and C. perfringens
type C being responsible for necrotic enteritis symptoms.
Clostridium perfringens toxinotypes correspond to a diverse
range of genotypes. The full genome sequence of C. perfringens
identified a total of 25 genes that contribute to the organism’s
virulence. Genotypes of the majority of strains include the plc
gene that encodes alpha toxin and, at the same time, none, one
or two genes encoding other type-specific exotoxins. Each
genotype may or may not carry the cpe gene. C. perfringens
exotoxin genes reside either on the chromosome or on large
plasmids that occur singly or in low copy numbers. Similarly,
the genome location of the gene encoding CPE may vary, with
the cpe gene residing on the chromosome in C. perfringens
strains associated with foodborne disease but positioned on a
plasmid in strains associated with nonfoodborne gastro-
intestinal disorders (e.g., antibiotic-associated or sporadic
gastroenteritis) or in strains of veterinary origin. When located
chromosomally, the cpe gene can be found on mobile genetic
elements, such as a lysogenized phage or a transposon.
Isolation and Identification
Quantitative recovery of viable C. perfringens cells from, and
detection of CPE in, food and/or patient specimens are key
steps for the diagnosis of C. perfringens gastroenteritis. In
addition, molecular methods are increasingly being used for
the detection of C. perfringens toxin genes and epidemiological
typing of C. perfringens isolates.
Conventional Methods
The procedure for enumeration of C. perfringens in meat is
based on initial recovery of microorganism on solid media for
sulfite-reducing anaerobes, followed by confirmation of col-
onies as C. perfringens with further biochemical tests.
Tryptose sulfite cycloserine (TSC) agar is the medium
presently recommended by both Association of Official Ana-
lytical Chemists (AOAC) International and the International
Organization for Standardization (ISO) for use in quantitative
recovery of C. perfringens. The initial selection is on TSC agar
with or without egg yolk. Egg yolk has traditionally been
added to media to enable detection of lecithinase activity
previously thought to be characteristic of C. perfringens.
However, it is now recognized that not all strains of C. per-
fringens are lecithinase-positive. Consequently, the lecithinase
reaction is not required as a differential property of the TSC
agar, and the egg yolk can be omitted. It should be noted,
however, that adding lysozyme or egg yolk to the medium
may enhance the recovery of thermally injured C. perfringens
spores. TSC agar contains the antibiotic cycloserine, which
suppresses the growth of facultative anaerobes. Ferric ammo-
nium citrate incorporated into the medium reacts with the
sulfide that is produced during sulfite reduction, forming a
black iron sulfide precipitate. Black colonies that develop
during incubation are reported as sulfite-reducing anaerobes.
ISO recommends that TSC agar be inoculated using the pour
plate method. Alternatively, the medium can be inoculated
using the spread plate method and overlayed with a small
volume of TSC agar. Incubation is at 37 °C under anaerobic
conditions.
Owing to the sensitivity of C. perfringens to low tempera-
tures, food samples to be tested for the presence of this
microorganism must not be refrigerated or frozen before an-
alysis. Instead, samples should be tested as soon as possible
after collection. However, activation of the heat-resistant
spores of C. perfringens is heat dependent and only approxi-
mately 4% of spores of food-poisoning strains will germinate
without prior heat shock. Patient specimens should be heat
treated before plating on TSC agar to maximize the recovery of
spores.
Isolates recovered from TSC agar are subsequently screened
with biochemical tests for motility, nitrate reduction, lactose
fermentation, and gelatin hydrolysis. Isolates that are non-
motile, reduce nitrate, ferment lactose, and hydrolyze gelatin
are identified as C. perfringens. Species-level identification of C.
perfringens can be achieved using commercially available
miniaturized test kits, for example, the RAPID ID 32A (bio-
Mérieux, Marcy-l'Etoile, France) or BBL Crystal Anaerobe kits.
Detection of C. Perfringens Enterotoxin
The detection of CPE in the stools of patients with food poi-
soning enables a definitive diagnosis of C. perfringens gastro-
enteritis to be made. CPE can be routinely detected in stool
specimens by enzyme-linked immunosorbent assay (ELISA)
and reverse passive latex agglutination (RPLA) assay. These
assays are capable of detecting as little as 2–4 ng g−1 CPE in
fecal material, well below the levels of 1 mg g−1 that are ex-
pected to occur in stool specimens from C. perfringens gastro-
enteritis patients. Even higher levels of assay sensitivity for CPE
detection can be achieved with Western immunoblotting.
Molecular Methods
A number of DNA-based methods exist for the detection
and identification of C. perfringens. These methods include
polymerase chain reaction (PCR) assays and gene probes
for the specific detection of the cpe gene to establish the
 Microbiological Safety of Meat | Clostridium perfringens
isolates ‘or foods’ potential for toxigenicity. Multiplex PCR has
been developed for simultaneous detection of several toxins,
including exotoxins and CPE, and this assay can be used to
replace conventional toxin typing. Recently, a duplex PCR
assay was described for differentiation of C. perfringens type A
isolates carrying chromosomal cpe genes from isolates carrying
this gene on a plasmid. DNA-based methods also include real-
time PCR and a PCR assay for the detection and/or identifi-
cation of C. perfringens using 16S rDNA-based specific primers.
Plasmid profiling, phage typing, ribotyping, pulsed-field
gel electrophoresis (PFGE), and amplification of fragment
length polymorphism (AFLP) analysis have been used for
tracing C. perfringens isolates from patients back to the out-
break food sources. While ribotyping, PFGE and AFLP each
demonstrate significant discriminatory power for strain-
specific differentiation of C. perfringens isolates, the genetic
diversity of C. perfringens strains and necessary expertise may
prove inhibitory for successful use of these methods in routine
epidemiological investigations. As both CPE-producing and
CPE-negative C. perfringens strains may possess indistinguish-
able fingerprints, it is recommended that before traceback
studies, the potential for CPE production by outbreak isolates
is established using a cpe gene detection assay.
Characteristics of C. Perfringens Foodborne Disease
In contrast to foodborne botulism, the symptoms of C. per-
fringens foodborne disease develop after ingestion of food
containing viable C. perfringens cells rather than preformed
toxins. C. perfringens type A gastroenteritis is usually charac-
terized by profuse diarrhea and cramping in the lower abdo-
men. The onset of the disease usually begins 6–12 h after the
ingestion of foods containing at least 4×109–6×109 C. per-
fringens vegetative cells (equivalent to 8–10 mg of CPE).
Vomiting and fever are uncommon. The symptoms lessen after
a further 24 h and usually resolve spontaneously. The mor-
tality rates associated with C. perfringens type A gastroenteritis
are low, but death may occur in immunocompromised pa-
tients, for example, the elderly. Gastroenteritis symptoms
caused by C. perfringens type A and Bacillus cereus are virtually
indistinguishable. Clostridium perfringens type C necrotic en-
teritis takes the form of severe gastroenteritis characterized by
bloody diarrhea, cramps, nausea, vomiting, and necrotic in-
flammation of the small intestine. The disease has a high
mortality rate of up to 25%.
Traditionally, a diagnosis of C. perfringens type A gastro-
enteritis was made on the basis of clinical signs and lesions as
well as quantitative recovery of C. perfringens from patient
specimens and food specimens. Clostridium perfringens was
typically verified as a causative agent of the disease when
(1) C. perfringens was present in implicated food at a level of
105 colony-forming units (CFU) g−1 or higher; (2) C. perfrin-
gens was present in patients’ stool samples at level of
106 CFU g−1 or higher; and (3) serotyping indicated similarity
of serotypes of C. perfringens strains isolated from food and
stools of patients. However, the traditional diagnostic scheme
has significant drawbacks, such as occasional carriage of C.
perfringens in stools of asymptomatic individuals at levels ap-
proaching those present in clinical specimens, or untypeability
337
with commercially available antisera of many outbreak strains
owing to the antigenic heterogeneity of C. perfringens. Con-
sequently, the criteria for diagnosis of C. perfringens type A
gastroenteritis were expanded to include evidence for the
presence of CPE in stool specimens of affected patients. More
recently, it was proposed that diagnosis may also be helped by
the detection of the cpe gene in food and fecal material, and by
establishing the chromosomal location of this gene in out-
break strains.
Mechanism of Pathogenicity
The events leading to pathological changes within the gastro-
intestinal tract that later manifest themselves as symptoms of
gastroenteritis are typically initiated with the ingestion of
vegetative cells of C. perfringens. It is thought that the majority
of these cells survive exposure to the acidic environment of
the stomach and start to multiply rapidly once the alkaline
environment of the small intestine is reached. Sporulation of
C. perfringens occurs readily in the presence of human intes-
tinal contents. CPE accumulates inside the cell during the
sporulation and is subsequently released into the lumen.
In the small intestine, CPE interacts with several proteins of
the epithelial cells. The toxin binds initially to a claudin pro-
tein receptor of the intestinal cell brush border and forms part
of a small, and then large, protein complex that becomes as-
sociated with the cell membrane. On formation of the large
complex, cell membrane permeability is affected, so that
leakage of small molecules occurs and, subsequently, synthesis
of DNA, RNA, and protein is inhibited. These changes result
directly in the death of the affected epithelial cells.
CPE induces a number of morphological changes in the
small intestine. The histopathological effects include for-
mation of blebs; shortening, desquamation, and necrosis of
the tips of the intestinal villi; and loss of the folded con-
figuration of the brush border. It is thought that the histo-
pathological damage is responsible for the disturbances to
fluid and electrolyte transport in the intestinal loops that
eventually manifest as acute diarrhea.
Epidemiology
Reservoirs of C. Perfringens
Clostridium perfringens is one of the most widely distributed
pathogenic bacteria and can be found in soil, dust, water,
and air of natural environments. Clostridium perfringens type A
occurs in soil at levels of 103–104 CFU g−1. Strains of C. per-
fringens known to cause gastroenteritis in humans are normal
inhabitants of the intestinal tract of humans and animals,
occurring in feces of healthy or asymptomatic individuals at
levels of up to 105 CFU g−1.
Food reservoirs of C. perfringens include raw beef, chicken
and pork, fresh and vacuum-packed fish and shellfish, raw fruit
and vegetables, soups, sauces and gravy mixes, cheese, and
spices. It is thought that approximately 50% of consumer-ready
items of raw meat and poultry contain C. perfringens. The or-
ganism may be found on the surface of beef, pork, and lamb
carcasses and is also recognized as an intrinsic organism
338 Microbiological Safety of Meat | Clostridium perfringens
present in the deep tissues or internal organs (spleen, liver,
kidneys or lymph nodes) of slaughter animals.
Traditionally, the widespread presence of C. perfringens in
the environment and foods was thought to explain the high
prevalence of C. perfringens type A food poisoning. However,
early surveys rarely identified the potential for toxigenicity
of clostridial isolates. Retrospective screening of C. perfringens
isolates showed that nearly half of the strains recovered dur-
ing outbreaks did not carry the cpe gene and were thus gen-
etically incapable of causing the disease. At present, it is esti-
mated that less than 5% of the total population of culturable
C. perfringens strains possess the cpe gene. Recently, none of the
C. perfringens isolates that were obtained in a comprehensive
survey of retail foods in the US was found to carry the cpe gene.
Consequently, high incidence rates obtained for C. perfringens
in foods and the environment may be of little relevance to
food safety. At present, the reservoirs for C. perfringens strains
that cause human gastroenteritis remain unknown. A novel
proposal is that humans are a source of enterotoxigenic
foodborne isolates.
Studies have indicated that despite the widespread presence
of C. perfringens in domestic animals, only a small proportion
of veterinary strains are CPE positive, carry the chromosomal
cpe gene, or produce heat-resistant spores. Depending on the
species, the incidence of C. perfringens strains capable of CPE
production in domestic animals in the US ranges from 0% to
22%, with prevalence in steers/heifers reaching 1.0% and that
in cows/bulls reaching 2.7%. Only a few of these CPE-positive
strains have a chromosomally located cpe gene. Consequently,
food animals have a lower potential for causing C. perfringens
gastroenteritis than was initially thought.
Characteristics of Outbreaks
Outbreaks of C. perfringens type A gastroenteritis typically
occur when meat or poultry containing C. perfringens spores
are cooked in advance, left to cool slowly with inadequate
refrigeration, and not reheated adequately before serving. The
dishes are usually prepared in a manner that favors the de-
velopment of anaerobic conditions, for example, as rolled
roasts or in large vats. The outbreaks are large, with a median
size of 25 or more cases, and frequently result from con-
sumption of food cooked by commercial catering companies.
Commercial meat processors are rarely implicated in out-
breaks of C. perfringens type A gastroenteritis.
It is thought that, under the conditions just described, heat-
resistant C. perfringens spores will survive and become acti-
vated during the cooking process. These spores will germinate,
outgrow, and multiply rapidly after the temperature of the
prepared dish falls below 50 °C and before it reaches ~15 °C.
The resulting vegetative cells, now present in the dish at
106–107 cells per gram, will not be destroyed in the absence of
adequate refrigeration and/or during inadequate reheating.
The usual vehicles for C. perfringens gastroenteritis out-
breaks are meat and poultry dishes. Between 1973 and 1987,
approximately 30% of C. perfringens outbreaks in the US were
associated with consumption of beef, whereas chicken and
turkey dishes accounted for approximately 15% of outbreaks.
More recently, meat and poultry dishes were confirmed as
vehicles in approximately one-third of all reported cases of
foodborne C. perfringens gastroenteritis in the US.
Incidence of the Disease
Of the three spore-forming bacteria most commonly associ-
ated with foodborne disease, that is, Bacillus cereus, Clostridium
botulinum, and C. perfringens, C. perfringens causes the most
outbreaks and cases. C. perfringens gastroenteritis is the second
most common cause of cases of bacterial foodborne disease in
the US after Salmonella.
In Europe also, C. perfringens gastroenteritis is the second
most common cause of foodborne disease after Salmonella. In
2000, 22% of deaths due to foodborne disease in England and
Wales were caused by C. perfringens. In the UK, the fall in the
numbers of cases and deaths due to C. perfringens gastro-
enteritis observed during the past decade is thought to be due
to a decline in the consumption of red meats.
In many countries, C. perfringens type A gastroenteritis is
not a notifiable disease. Because of lack of adequate reporting,
the incidence of this disease and its economic impact are likely
to be underestimated.
Control and Preventive Measures
A number of factors contribute to the ability of C. perfringens to
cause outbreaks of foodborne disease. Of these factors, its
widespread presence in foods and the environment, its for-
mation of heat-resistant spores and its short generation times
significantly influence the approach to control of this micro-
organism, and the disease it causes.
Because C. perfringens is prevalent in the farm environment,
the organism is frequently detected in slaughter animals, on
dressed carcasses and in abattoir environments. Traditionally,
it was thought that during slaughter and dressing, carcasses
inevitably became contaminated with C. perfringens spores
because of their transfer to the carcass as opening cuts are
made in the skin. Consequently, the possibility of raw meat
being free from C. perfringens was thought to be unrealistic and
its presence in meat was regarded as unavoidable. Now it is
recognized that only a small proportion of C. perfringens
strains from food animals and abattoir environments are
capable of causing foodborne disease, control of carcass/cut
contamination with C. perfringens spores may become feasible,
by identification of farm and/or abattoir reservoirs of con-
tamination with outbreak strains. Once these reservoirs are
identified, specific control measures can be developed to re-
duce the initial contamination of raw meat and eliminate
transfer of clostridial spores to processed meats. Similarly,
following the identification of reservoirs of foodborne disease-
causing C. perfringens strains, control measures could be dir-
ected at specific operations within the retail sector, commercial
catering facilities, and/or food industries.
In the past, removal or inactivation of C. perfringens spores
present on carcasses or cuts proved unsuccessful. Unless extreme
measures are employed, various carcass decontamination
treatments frequently result in only approximately 1 log re-
ductions in the levels of C. perfringens spores. With the high
 Microbiological Safety of Meat | Clostridium perfringens
D95 °C values of some strains, the use of thermal treatments to
destroy C. perfringens spores without impairing the desired
organoleptic attributes and palatability of prepared foods is
generally not possible.
Traditionally, the approach to control of C. perfringens type
A gastroenteritis centered on inhibiting the multiplication of
the organism in food. The most practical way of preventing
C. perfringens gastroenteritis appears to be by preparing meat
and poultry dishes shortly before they are served, and by
adequate cooling, refrigeration, and reheating of cooked
products. The USDA guidelines recommend that cooked meat
dishes are cooled from an internal temperature of approxi-
mately 54 °C to approximately 27 °C within less than 1.5 h,
and from approximately 27 °C to approximately 4 °C within
less than 5 h in order to avoid multiplication of C. perfringens.
Following cooling, food should be stored refrigerated, and
should be reheated immediately before serving to reach an
internal temperature of 70 °C or above.
Interestingly, regardless of initial contamination of the raw
material, times and temperatures employed during cooking
of food and cooling rates achieved for the cooked product,
C. perfringens type A gastroenteritis could be avoided if food
was reheated to 70 °C before serving. It seems that regardless
of the other, various possibilities for control of C. perfringens
during food manufacturing, education of food service workers
remains paramount for effective prevention of C. perfringens
foodborne disease.
See also: Microbiological Analysis: DNA Methods; Standard
Methods
Further Reading
De Jong, A., Baumer, R., Rombouts, F., 2002. Optimizing sporulation of Clostridium
perfringens. Journal of Food Protection 65, 1457–1462.
Food and Drug Administration. 2011. Clostridium perfringens. Bacteriological
Analytical Manual (Chapter 16). Available from http://www.fda.gov/Food/
ScienceResearch/LaboratoryMethods/BacteriologicalAnalytical
ManualBAM/default.htm (accessed 11.10.13).
339
Gao, Z., McClane, B., 2012. Use of Clostridium perfringens enterotoxin and the
enterotoxin receptor-binding domain (C-CPE) for cancer treatment: Opportunities
and challenges. Journal of Toxicology. doi:10.1155/2012/981626.
Grant, K., Kenyon, S., Nwafor, I., et al., 2008. The identification and characterization
of Clostridium perfringens by real-time PCR, location of enterotoxin gene and
heat resistance. Foodborne Pathogens and Disease 5, 629–639.
Heikinheimo, A., Lindstrom, M., Liu, D., Korkeala, H., 2010. Clostridium. In: Di, L.
(Ed.), Molecular Detection of Foodborne Pathogens. Boca Raton, FL: CRC Press,
pp. 145–156.
International Organization for Standardization, 2004. Microbiology of Food and
Animal Feeding Stuffs-Horizontal Methods for the Enumeration of Clostridium
perfringens − Colony Count Technique. Geneva: International Organization for
Standardization ISO 7937:2004.
Labbe, R., Grant, K., 2011. Clostridium perfringens in food service. In: Hoorfar, J.
(Ed.), Rapid Detection, Characterization, and Enumeration of Foodborne
Pathogens. Washington, DC: ASM Press, pp. 381–392.
Labbe, R., Heredia, N., 2013. Clostridium perfringens. In: Labbe, R., Garcia, S.
(Eds.), Guide to Foodborne Pathogens, second ed. London: Wiley and Sons.
Li, J., McClane, B., 2006. Further comparisons of temperature effects on growth and
survival of Clostridium perfringens type A isolates carrying a chromosomal or
plasmid-borne enterotoxin gene. Applied and Environmental Microbiology 72,
4561–4568.
Lin, Y.-T., Labbe, R., 2003. Enterotoxigenicity and genetic relatedness of Clostridium
perfringens isolates from retail foods in the United States. Applied and
Environmental Microbiology 69, 1642–1646.
Lindstrom, M., Heikinheimo, A., Lahti, P., Korkeala, H., 2011. Novel insights into
the epidemiology of Clostridium perfringens type A food Poisoning. Food
Microbiology 28, 192–198.
McClane, B., 2007. Clostridium perfringens. In: Doyle, M., Beuchat, L. (Eds.), Food
Microbiology, Fundamentals and Frontiers, third ed., pp. 423–444. Washington,
DC: ASM Press, pp. 423–444.
Miki, Y., Miyamoto, K., Kaneko-Hirano, I., Fujiuchi, K., Akimoto, S., 2008.
Prevalence and characterization of enterotoxin gene-carrying Clostridium
perfringens isolates from retail meat products in Japan. Applied and
Environmental Microbiology 74, 5366–5372.
Scallan, E., Hoekstra, R., Angulo, F., et al., 2011. Foodborne illness in the United
States − major pathogens. Emerging Infectious Diseases 17, 7–15.
USDA/FSIS, 2001. U.S. Department of Agriculture, Food Safety and Inspection
Service. Performance standards for the production of certain meat and poultry
products; final rule. Federal Register 64, 732–749.
Relevant Websites
http://www.fda.gov/Food/FoodborneIllnessContamination/default.htm
Foodborne Illness and Contaminants.
http://www.fda.gov/food/foodscienceresearch/laboratorymethods/ucm2006949.htm
U.S. Food and Drug Administration.