Clostridium botulinum and Botulism
JW Austin, Tunney’s Pasture, Ottawa, ON, Canada
r 2014 Elsevier Ltd. All rights reserved.
This article is a revision of the previous edition article by JA Boerema,
DM Broda, volume 2, pp 786–793, © 2004, Elsevier Ltd.
Botulism
Foodborne botulism is an intoxication resulting from con-
sumption of foods in which Clostridium botulinum has grown
and produced toxin. Depending on the amount of toxin in-
gested, the onset of botulism usually begins 18–36 h after
ingesting toxin-containing food. As with other bacterial food-
borne illnesses, the initial symptoms may include diarrhea and
vomiting. Botulinum intoxication results in a descending
symmetrical flaccid paralysis. Cranial nerves are affected ini-
tially, resulting in one or more of blurred and double vision,
fixed and dilated pupils, ptosis (drooping eyelids), dysphonia
(difficulty swallowing), dysphagia (difficulty speaking), and
dry mouth. Paralysis may descend causing muscle weakness
and paralysis affecting the diaphragm. Fatal cases are normally
the result of respiratory failure. Botulism is frequently con-
fused with other illnesses, especially in geographical areas
where the disease has a low incidence. The symptoms of
botulism are commonly confused with Guillain–Barré syn-
drome, stroke, and myasthenia gravis.
A diagnosis of botulism can be made by demonstration of
botulinum neurotoxin in the patient's serum or the toxin and/
or the organism in feces. As C. botulinum is not normally part
of the human intestinal microflora, its isolation from feces or
gastric contents, in association with classic symptoms of the
disease, is diagnostic. Owing to improved medical care, such
as the use of respiratory support systems and timely ad-
ministration of antitoxin, the fatality rate due to botulism has
fallen significantly in recent years.
In Europe, more than 2500 cases of foodborne botulism
were reported in 1999–2000. Countries with a high reported
incidence include Armenia, Azerbaijan, Belarus, Georgia, Pol-
and, Russia, Turkey, and Uzbekistan. A smaller but significant
number of cases are reported annually in France, Germany,
Italy, China, and the USA. It should be noted that the true
incidence of foodborne botulism is likely to be much higher,
with underreporting being an issue. Foodborne botulism is
not reportable in all countries and the efficiency with which
potential outbreaks are investigated varies from country to
country.
Being described first in 1976, infant botulism has become
the most commonly reported form of botulism in the US, with
approximately 80–100 cases occurring annually. Unlike
foodborne botulism, infant botulism is caused by ingestion of
spores, followed by colonization of the intestinal tract by C.
botulinum, with in situ production of neurotoxin. A third form
is wound botulism, wherein the organism infects tissue and
produces toxin at a wound site. With no cases being reported
in the UK before 2000, wound botulism has now become the
most common form of botulism in the UK as a result of in-
jection of illicit drugs. As only foodborne botulism relates to
330
the microbiological safety of meat, further discussion will be
limited to that type of illness.
Foodborne botulism is likely as old as food preservation.
‘Sausage poisoning’ was first seriously studied following an
outbreak in Wildbad, Germany, in 1793, which resulted in 13
cases with 6 deaths. Although originally attributed to bella-
donna poisoning (caused by consumption of leaves or berries
of the Nightshade plant), it was more widely accepted that the
cause was consumption of a locally produced blood sausage
‘Blunzen,’ which was a pig stomach filled with blood and
other ingredients, briefly boiled, and preserved by smoking.
Following the Wildbad outbreak, the number of reported cases
of sausage poisoning rapidly increased, prompting an 1829
study of the disease by the local health officer, Justinius Kerner,
who described 230 cases of sausage poisoning over a period of
25 years. The illness became known as ‘botulism’ after ‘botulus,’
the Latin word for sausage. Kerner's report was the first pub-
lished complete description of the clinical symptoms of
foodborne botulism.
An outbreak of botulism involving 34 cases caused by
salted ham served at a gathering of amateur musicians in
Ellezelles, Belgium, occurred in December 1895. The outbreak
was investigated by Prof. E. Van Ermengem of the University of
Ghent. Van Ermengem reported that portions of ham fed to
mice, guinea pigs, and monkeys caused flaccid paralysis and
death. Filtered extracts of ham had the same effects as ma-
cerated ham. Van Ermengem found an anaerobic sporulating
bacillus, which was named Bacillus botulinus, in cultures of the
ham as well as a culture of spleen from a deceased victim.
Cultures and culture filtrates had the same effects as the ma-
cerated ham and ham filtrates, indicating involvement of a
filterable toxin that was produced by the bacterium. In the
investigation of this outbreak, Van Ermengem established
that botulism was an intoxication, not an infection, and the
toxin was produced by a spore-forming obligately anaerobic
bacterium.
C. botulinum
Clostridium botulinum is the ‘species’ name assigned to an as-
semblage of anaerobic, spore-forming, rod-shaped bacteria, all
of which produce botulinum neurotoxin that causes the severe
neuroparalytic condition known as botulism. Morpho-
logically, members of the C. botulinum assemblage are Gram-
positive, anaerobic, motile rods, 4–6 mm by 0.9–1.2 mm in size
with oval, subterminal spores (Figure 1).
Originally, all organisms known to produce botulinum
neurotoxin were included in this species. There are seven types
of C. botulinum, A through G, based on the serological speci-
ficity of the neurotoxin produced. Human botulism, including
foodborne, wound, and infant botulism, is associated with
Encyclopedia of Meat Sciences, Volume 2 doi:10.1016/B978-0-12-384731-7.00036-2
 Microbiological Safety of Meat | Clostridium botulinum and Botulism 331

cause animal botulism. These strains are nonproteolytic, grow

optimally at 40 °C, and do not grow at temperatures less than
15 °C. Group IV strains, which produce type G neurotoxin,
grow optimally at 37 °C and have a minimal growth tem-
perature of 10 °C.
These four groups, plus neurotoxin-producing strains of
Clostridium butyricum type E and Clostridium baratii type F,
make a total of six distinct genomic groups that produce
botulinum neurotoxin. With a few exceptions, infant botulism
is caused by proteolytic strains of C. botulinum. In the few
exceptional cases, other clostridia (C. baratii producing type F
toxin and C. butyricum producing type E toxin) have been
implicated.

Figure 1 A transmission electron microsgraph of a thin section Isolation and Characterization of C. botulinum
through several vegetative cells and spores of Clostridium botulinum.
Bar represents 2 mm.
The diagnosis of foodborne botulism is generally confirmed if,
in addition to the clinical syndrome, botulinum toxin and/or
types A, B, E, and F. Types C and D cause botulism in animals.
viable C. botulinum are detected in a suspect food or a clinical
To date, there is no direct evidence linking type G to the
specimen. Suitable specimens for toxin analysis are serum,
disease.
feces, enema fluid, and stomach contents. The same speci-
The species is also divided into four groups on the basis of
mens, except serum, are also suitable for the detection of C.
physiological and genomic differences. Strains belonging to
botulinum. Botulinum toxin is detected by injecting serum or
group I include all type A strains and proteolytic strains of
extracts from foods and clinical specimens into mice, and then
types B and F. Clostridium botulinum Group II includes all type
observing them for characteristic symptoms including ruffled
E strains and nonproteolytic strains of types B and F. Clos-
fur, labored breathing, and a pinched waist. These symptoms,
tridium botulinum Group III includes all type C and D strains.
combined with the absence of these symptoms in specimens
Clostridium botulinum group IV, or C. botulinum type G, has
neutralized with specific antisera, can be considered an earlier
been renamed Clostridium argentinense. A high degree of re-
endpoint for the mouse assay negating the requirement for
latedness exists among strains within each group, but there is
death as an endpoint.
little relatedness between groups.
The detection of C. botulinum involves anaerobic incu-
Group I strains are proteolytic and are typified by strains
bation of foods and clinical specimens in liquid media, and
that produce neurotoxin type A. The optimal temperature for
then subsequent toxin analysis. In major outbreaks or in the
growth is 37 °C, with growth occurring between 10 °C and
isolation of uncommon serotypes, the analyses are followed
48 °C. High levels of neurotoxin are typically produced in
by the isolation of the incriminated microorganism. The cus-
cultures. Spores of proteolytic strains are resistant to heat, with
tomary procedure for isolation of C. botulinum from food is
D100 °C values of approximately 25 min (the D value is the
based on an enrichment procedure followed by detection and
time required to inactivate 90% of the population at a given
serotyping of toxin in culture supernatant fluid. Commonly
temperature). To inhibit growth, the pH must be less than 4.6,
used enrichment procedures include preliminary heat or
salt concentration more than 10%, or the water activity (aw)
ethanol treatments to destroy competing nonsporing bacteria,
less than 0.94.
followed by anaerobic culture in media such as cooked meat
Group II strains are nonproteolytic, have a lower optimum
medium or trypticase-peptone-glucose-yeast extract broth.
growth temperature (30 °C), and are psychrotolerant, that is to
Enrichment incubation is normally at temperatures between
say, being capable of growth at temperatures as low as 3.0 °C.
26 °C and 35 °C for 5–10 days. A selective and differential agar
The spores have a much lower heat resistance than those of
medium containing antibiotics and egg yolk may be used for
group I strains, with D100 °C values less than 0.1 min. Group II
isolation of the organism from enrichment broth.
strains are inhibited at pH less than 5.0, salt concentrations
more than 5%, or water activities (aw) less than 0.97. The
original strain isolated by van Ermengem in 1895 was prob-
ably nonproteolytic C. botulinum type B, and many type B cases Botulinum Neurotoxin
in Europe are still due to strains of nonproteolytic C. botuli-
num. Recorded outbreaks of botulism involving non- The specificity of botulinum toxin for neurons makes it ex-
proteolytic C. botulinum have most frequently been associated quisitely toxic. The lethal dose of botulinum toxin for a 70 kg
with meat, fish (e.g., salted, dried, vacuum, or smoked), and human is estimated to be approximately 0.09–0.15 mg intra-
homemade foods prepared by the peoples of Alaska and venously or intramuscularly and 70 mg orally. Following in-
northern Canada, such as aged beaver tail and paw, aged sal- gestion, the toxin is absorbed through the gastric and upper
mon roe and ‘muktuk’ (i.e., whale skin and fat). intestinal mucosa from where it enters the bloodstream. Botu-
Group III includes strains producing types C and D linum neurotoxin then gains access to the nervous system,
neurotoxins, which are not involved in human botulism but where it blocks the release of the neurotransmitter acetylcholine,
332 Microbiological Safety of Meat | Clostridium botulinum and Botulism
preventing muscle contraction and thereby causing flaccid
paralysis.
The active toxins are first synthesized as single polypeptides
with low activity that require posttranslational proteolytic
cleavage to form the active dichain molecule consisting of
heavy and light chains joined together by a disulfide bridge.
Strains of Group I C. botulinum are proteolytic and self-activate
the toxin with endogenous proteases. However, Group II
strains, all of which are considered nonproteolytic, need ex-
ogenous proteolytic enzymes or trypsin treatment to activate
the toxin. The toxin is stable in acidic conditions (pH 3.5) but
is easily inactivated in slightly alkaline conditions. The toxin is
heat labile; consequently, normal cooking procedures should
ensure a food's safety with respect to botulism. However,
freezing does not destroy the toxin.
Incidence of C. botulinum in Meats
Spores of proteolytic and nonproteolytic C. botulinum are
widespread in nature and are found in soils, aquatic sedi-
ments, and the gastrointestinal tracts of animals. Given the
ubiquitous nature of C. botulinum spores, their presence in
meats must be assumed and appropriate controls to prevent
growth and toxin production must be applied. Information
regarding the prevalence rates for C. botulinum on meat is not
readily available, mainly because of the cost and difficulties of
detecting C. botulinum in foods. However, the studies that have
been done indicate that the incidence and levels of C. botuli-
num in meats are low, compared with fish and fishery prod-
ucts. Several studies indicate that the incidence of C. botulinum
in meat samples is often less than 10%, with levels at ap-
proximately 1 spore per kg. The more frequent occurrence of
botulism acquired from pork than from other meat products
suggests more frequent contamination of pork than that of
beef, lamb, and other meats. Toxin type B is typically impli-
cated in cases of meat-borne botulism. Survey results reveal
that nearly all toxin types identified from raw and semi-
preserved meats were either A or B. The finding of low num-
bers of spores of C. botulinum in pig and cattle's feces indicates
that clinically healthy animals occasionally carry C. botulinum
spores. Thus, the contamination of carcasses with C. botulinum
spores during carcass dressing seems likely.
Botulism Incidents Involving Meat Products
Home processing of meat is more common in continental
Europe than in the UK or North America and an increased
incidence of foodborne botulism, most frequently associated
with meat products, has been observed in eastern European
countries. Nonproteolytic type B strains are the etiological
agents in most outbreaks of botulism in Germany, France, and
Portugal that have been caused by home-prepared salted or
cured hams. Homemade bottled pork meat is the main vehicle
of botulism in Poland. Three incidents occurring in the UK
and Ireland involved Polish nationals and were associated
with the consumption of home-prepared meat products ori-
ginating from Poland. Of 106 cases of botulism in Romania
diagnosed during 2007–09, 86 (81.1%) were associated with
the consumption of home-prepared pork products (ham,
bacon, blood pudding, mosaic salami, raw sausages, and
smoked-dried meat), whereas commercially canned products
were involved in 20 cases (18.9%).
Most cases of botulism due to meat products in North
America result from consumption of traditional northern
foods by Inuit or Eskimos. Peccant foods include meat and fat
from seal, whale, walrus, and beaver. Other than these
northern foods, botulism from meat products is rare in Can-
ada and the US. Commercial pate was the cause of two cases of
botulism in Quebec in 1995, whereas commercial jarred pork
caused a single case in Quebec in 2001. In July of 2007, an
outbreak from commercially canned hotdog chili sauce caused
10 cases of botulism in Texas and Indiana. A 15-case botulism
outbreak, also caused by chili, occurred in Texas in 2001. As
both these cases involved chili, a food with several ingredients,
it was not determined whether meat, or another ingredient,
contributed the spores. Occasional single cases were reported
in the US from home-prepared foods including stew and
home-canned beef and peas; however, in these cases, it is also
impossible to determine whether meat was the responsible
ingredient.
Although home and artisanal production remain the
principal causes of botulism outbreaks, the proportion of cases
attributable to commercial products is increasing, especially in
Europe, where recent outbreaks have been linked to widely
distributed, commercially produced foods. Methods for pre-
serving food products are changing, and fresh products that are
vacuum-packed and refrigerated with extended shelf-lives, or
products that are heat treated at temperatures and times too
mild to inactivate C. botulinum spores, are increasing the risk of
botulism from commercial foods.
Control of C. botulinum in Meats
Safe food production is based on either destroying spores of
C. botulinum using a thermal process or inhibiting growth of
the organism in foods, in combination with low storage
temperatures and limited storage times. Incorporation of a
combination of inhibitory factors such as reduced pH or water
activity, added preservatives, and competing microflora pro-
vide multiple barriers and help processors to achieve a safe
product. In addition to inhibition of growth of C. botulinum,
the microbiological safety of foods also relies on good control
and monitoring of processes throughout manufacture and
distribution.
Refrigeration
The psychrotolerant nature of nonproteolytic strains of C.
botulinum makes these strains of particular concern in re-
frigerated products. Psychrotrophic C. botulinum has the ability
to survive mild heat treatment of minimally processed foods
and may grow during cold storage. Growth of psychrotrophic
C. botulinum occurs in response to extrinsic parameters such as
storage at temperatures and redox potentials permissive for
growth and parameters intrinsic to the food, such as pH and
water activity.
 Microbiological Safety of Meat | Clostridium botulinum and Botulism
Toxin formation by C. botulinum is both time and tem-
perature dependent. At its lowest growth temperatures, it takes
a C. botulinum strain many weeks to produce toxin. However, a
slight rise in incubation temperature is accompanied by a
rapid increase in growth rate of C. botulinum and a reduction in
time to toxin detection. Storage of foods for several weeks at
refrigeration temperatures is needed for toxigenesis by non-
proteolytic strains. Thus, refrigerated products with a short
shelf-life normally would not present significant risk. How-
ever, products with extended shelf-lives stored at refrigeration
temperatures for extended periods may produce toxin by
nonproteolytic strains of C. botulinum.
As strict temperature control of refrigerated products is
often not maintained during their storage, distribution, dis-
play, and subsequent handling in domestic, food service, or
institutional facilities, the likelihood of toxin production by
nonproteolytic strains of C. botulinum in extended shelf-life
products is increased. However, low-temperature storage can-
not be reliably used as the sole means of controlling growth
and toxin production by C. botulinum.
Consumer demands for ready-to-eat convenience foods,
combined with an emphasis on little or no preservatives and
less processing, have placed a new focus on C. botulinum. The
lack of a heat treatment sufficient to destroy spores of C.
botulinum, use of packaging that mostly or totally exclude
oxygen, prolonged storage at chill temperatures, and the lack
of heating before consumption combine to increase the risk of
botulism from these foods. These products often do not use
additional preservative systems such as reduced pH or water
activity. In those foods where such treatment would adversely
affect product quality, other controls, such as reduced water
activity or acidification, should be considered. Subinhibitory
levels of several factors can be combined to control growth of
C. botulinum by application of what is known as the hurdle
concept.
Thermal Processing
A great number of botulism outbreaks during the early twen-
tieth century in Europe and North America were associated
with the widening use of canning and bottling processes to
extend shelf-life. This led to the development and enforcement
of the ‘botulinum cook’ for commercial processing. The
‘botulinum cook’ was developed as a heat process for low acid
foods (4pH 4.6) in order to destroy the spores of C. botuli-
num, and its widespread use led to substantial reductions in
the number of botulism outbreaks. Spores are a dormant form
of the organism that are resistant to high temperatures, high
pressure, UV light, and desiccation. The ‘botulinum cook’
process is designed to reduce the population of the most re-
sistant C. botulinum spores to 10–12 of their original numbers.
The decimal reduction time (D value) is the time in minutes at
a given temperature in order to produce a one log reduction in
C. botulinum spore number. Much higher temperatures are
required to inactivate spores of Group I strains, compared with
those of Group II. Group I strains typically have D values in
the range of 0.21 min at 121 °C, whereas Group II strains have
D values of 2.4 min at 82.2 °C. Botulism in canned foods re-
sults from underprocessing or postprocess contamination. In
333
the case of underprocessing, it is the heat-resistant proteolytic
strains that are of concern with regard to product safety.
C. botulinum is controlled in shelf-stable canned meats using
thermal processing.
Redox Potential and Atmosphere
C. botulinum is a strict anaerobe. However, even within foods
exposed to oxygen, the redox potential is often low enough to
support the growth of this organism. Vacuum packaging and
modified atmosphere packaging were developed for the ex-
tension of product shelf-life, but concerns have been raised
about risks from these products with respect to botulism. In
modified atmosphere packaging of certain meat products, the
air in the headspace of the package is replaced by CO2 and N2,
resulting in a low O2 environment. There is concern about the
safety of these products with respect to the potential for
growth and toxin production by nonproteolytic C. botulinum.
Vacuum or modified atmosphere packaging in atmospheres
without O2 restricts the growth of aerobic spoilage bacteria but
not of clostridia or other anaerobic bacteria. There have been a
number of reports describing low temperature spoilage of
vacuum-packaged meats caused by psychrotolerant Clostridium
spp. These incidents demonstrate that conditions within a
chilled vacuum pack may select for the growth of psychroto-
lerant clostridia. Outbreaks of type E botulism in the 1960s
were linked to vacuum-packed smoked fish. Studies have
shown no difference in the rate of toxin production in high-
and low-oxygen barrier films. However, it is of concern that
the use of high-barrier oxygen film may increase the organo-
leptic acceptability of a toxic product. Inhibition of competing
organisms may permit toxin production by C. botulinum in
refrigerated modified atmosphere packaged foods without
obvious sensory evidence of spoilage.
pH
C. botulinum will not grow in highly acidic foods that have a
pH value less than 4.6. Consequently, acidification is widely
used to control the growth of C. botulinum in food products.
Cases of botulism have been linked to the consumption of
high-acid foods in which the growth of yeasts or molds has
raised the pH sufficiently to allow the growth of C. botulinum.
In general, proteolytic strains of C. botulinum are more tolerant
of acidic conditions than the nonproteolytic strains.
Water Activity
The generally accepted minimum aw for growth of C. botulinum
in foods, under otherwise optimal conditions, is 0.94 and 0.97
for proteolytic and nonproteolytic strains, respectively. The
values 0.94 and 0.97 correspond to salt concentrations of
approximately 10% and 5%, respectively. Today, high salt
concentrations in foods are unacceptable to most consumers.
Lower salt concentrations can, however, be effective when used
in combination with other inhibitory factors such as pH and
nitrite.
334 Microbiological Safety of Meat | Clostridium botulinum and Botulism
Preservatives
Nitrite
Sodium nitrite is a multifunctional food additive, responsible
for the characteristic color and flavor associated with cured
meats and at the same time providing protection against
growth and toxin formation by C. botulinum in cured meats
subjected to temperature abuse. The exact mechanism of
botulinum inhibition by nitrite is not known. Its efficacy de-
pends on interactions involving pH, salt, heat treatment,
storage temperature and time, and the composition of the
food matrix. It has been shown that nitrite interacts with ni-
trogenous compounds to form carcinogenic nitrosamines and
intestinal bacteria mediate the formation of nitrosamines in
the body. As a result, in recent years, consumer and regulatory
pressure has mounted to reduce the levels of nitrite in pro-
cessed meats. The maximum concentration of sodium nitrite
(NaNO2) in meat products typically is 150 mg kg–1. C. botu-
linum in cured meat products is primarily controlled by re-
frigeration and the use of nitrite. The control measure to apply
is the addition of a sufficient quantity of nitrite salt (defined by
the sodium nitrite (NaNO2) concentration).
Nisin
Bacteriocins, antimicrobial peptides that inhibit the growth of
a broad spectrum of Gram-positive microorganisms, offer a
natural alternative as biopreservatives for safeguarding min-
imally processed foods. Nisin is a peptide antibiotic produced
by some strains of Lactococcus lactis. It has been used as a food
preservative in many countries for more than 50 years and has
been granted generally regarded as safe status. Nisin is not only
active against closely related lactic strains but is also effective
for inhibiting the growth of the foodborne pathogens Listeria
monocytogenes, Staphylococcus aureus, and C. botulinum under
certain conditions. Nisin sensitivity varies among C. botulinum
strains. Growth conditions and food components also affect
nisin's effectiveness. Factors decreasing nisin's ability to inhibit
C. botulinum growth include a low-acid environment and high
protein and phospholipid concentrations in foods.
Competing Microorganisms
In most foods, competing organisms, when present, often
grow more rapidly than C. botulinum, as this microorganism is
a poor competitor. The growth of organisms such as the lactic
acid bacteria lowers the pH and, consequently, inhibits the
growth of C. botulinum. Strains of lactic acid bacteria have been
found to produce bacteriocins (low molecular weight pro-
teins) that are inhibitory to C. botulinum. These strains hold
promise for use in the food industry, where they may provide
‘natural’ protection against C. botulinum hazards.
Hurdle Technology
Although hurdles to growth of C. botulinum have been re-
viewed separately, they are typically used in combination.
Thermal processing resulting in a 12 log reduction of C. botu-
linum spores, although acceptable for canned foods, would
render many meat products inedible. Reliance on refrigerated
storage alone results in the risk that a food may be temperature
abused.
Perishable meat products rely on chilling, in combination
with intrinsic factors, in order to control growth of C. botuli-
num. Products such as luncheon meats in hermetically sealed
containers receive a mild heat treatment but remain shelf
stable due to refrigerated storage, and nitrites and salt are
added to inhibit growth of C. botulinum. Bacon and some
fermented, undried sausages are preserved by chilling, in
combination with nitrite, and reduced water activity and pH.
Shelf-stable meat products rely on intrinsic factors to pre-
vent growth of C. botulinum. For example, Italian mortadella
relies on a combination of a thermal process, reduced water
activity, low pH, and the addition of nitrite and smoke. Other
meat products rely more on a limited number of hurdles. For
example, canned unsalted meat relies only on the thermal
process, whereas Parma-type ham relies primarily on reduction
of water activity with salt, with a lesser reliance on reduced pH.
See also: Biopreservation. Canning. Chemical Analysis for
Specific Components: Curing Agents. Microbiological Safety of
Meat: Hurdle Technology
Further Reading
Austin, J.W., Leclair, D., 2011. Botulism in the North: a disease without borders.
Clinical Infectious Diseases 52, 593–594.
Emanuelle, E., Vaillant, V., de Valk, H., Popoff, M.R., 2003. France recalls
internationally distributed halal meat products from the plant implicated as the
source of a type B botulism outbreak. Eurosurveillance 7 (38), 2295.
Fagan, R.P., McLaughlin, J.B., Castrodale, L.J., et al., 2011. Endemic foodborne
botulism among Alaska Native persons − Alaska, 1947–2007. Clinical Infectious
Diseases 52, 585–592.
Lucke, F.-K., Roberts, T.A., 1993. Control in meat and meat products. In: Hauschild,
A.H.W., Dodds, K.L. (Eds.), Clostridium botulinum. Ecology and Control in
Foods. New York: Marcel Dekker, pp. 177–207.
Neghina, A.M., Marincu, I., Moldovan, R., Iacobiciu, I., Neghina, R., 2010.
Foodborne botulism in southwest Romania during the post-communism period
1990−2007. International Journal ofInfectious Diseases 14, 96–101.
Neghina, A.M., Neghina, R., 2011. Epidemiology of foodborne botulism in Romania
1980−2009. Foodborne Pathogens and Diseases 8, 907–911.
Peck, M.W., Stringer, S.C., 2005. The safety of pasteurised in-pack chilled meat
products with respect to the foodborne botulism hazard. Meat Science 70 (3),
461–475.
Peck, M.W., Stringer, S.C., Carter, A.T., 2011. Clostridium botulinum in the post-
genomic era. Food Microbiology 28, 183–191.