Species of endospore forming bacterium
Clostridium botulinum
is a
gram-positive
,
[1]
rod-shaped
,
anaerobic
,
spore-forming
,
motile
bacterium
with the ability to produce
botulinum toxin
, which is a
neurotoxin
.
[2]
[3]
C. botulinum
is a diverse group of
pathogenic bacteria
. Initially, they were grouped together by their ability to produce botulinum toxin and are now known as four distinct groups,
C. botulinum
groups I?IV. Along with some strains of
Clostridium butyricum
and
Clostridium baratii
, these bacteria all produce the toxin.
[2]
Botulinum toxin can cause
botulism
, a severe
flaccid paralytic
disease in humans and other animals,
[3]
and is the most potent toxin known to science, natural or synthetic, with a lethal dose of 1.3?2.1 ng/kg in humans.
[4]
[5]
C. botulinum
is commonly associated with bulging
canned
food; bulging, misshapen cans can be due to an internal increase in pressure caused by gas produced by bacteria.
[6]
C. botulinum
is responsible for foodborne
botulism
(ingestion of preformed toxin), infant botulism (intestinal infection with toxin-forming
C. botulinum
), and wound botulism (infection of a wound with
C. botulinum
).
C. botulinum
produces heat-resistant
endospores
that are commonly found in soil and are able to survive under adverse conditions.
[2]
Microbiology
[
edit
]
C. botulinum
is a
Gram-positive
, rod-shaped, spore-forming
bacterium
.
[1]
It is an
obligate anaerobe
, the organism survives in an environment that lacks
oxygen
. However,
C. botulinum
tolerates traces of oxygen due to the enzyme
superoxide dismutase
, which is an important antioxidant defense in nearly all cells exposed to oxygen.
[7]
C. botulinum
is able to produce the neurotoxin only during sporulation, which can happen only in an anaerobic environment.
C. botulinum
is divided into four distinct
phenotypic
groups (I-IV) and is also classified into seven
serotypes
(A?G) based on the
antigenicity
of the botulinum toxin produced.
[8]
[9]
On the level visible to DNA sequences, the phenotypic grouping matches the results of whole-genome and
rRNA
analyses,
[10]
[11]
and setotype grouping approximates the result of analyses focused specifically on the toxin sequence. The two
phylogenetic trees
do not match because of the ability of the toxin
gene cluster
to be horizontally transferred.
[12]
Serotypes
[
edit
]
Botulinum neurotoxin
(BoNT) production is the unifying feature of the species. Seven
serotypes
of
toxins
have been identified that are allocated a letter (A?G), several of which can cause disease in humans. They are resistant to degradation by enzymes found in the gastrointestinal tract. This allows for ingested toxins to be absorbed from the intestines into the bloodstream.
[5]
Toxins can be further differentiated into subtypes on the bases of smaller variations.
[13]
However, all types of botulinum toxin are rapidly destroyed by heating to 100 °C for 15 minutes (900 seconds). 80 °C for 30 minutes also destroys BoNT.
[14]
[15]
Most strains produce one type of BoNT, but strains producing multiple toxins have been described.
C. botulinum
producing B and F toxin types have been isolated from human botulism cases in
New Mexico
and
California
.
[16]
The toxin type has been designated Bf as the type B toxin was found in excess to the type F. Similarly, strains producing Ab and Af toxins have been reported.
[12]
Evidence indicates the neurotoxin genes have been the subject of
horizontal gene transfer
, possibly from a viral (
bacteriophage
) source. This theory is supported by the presence of integration sites flanking the toxin in some strains of
C. botulinum
. However, these integrations sites are degraded (except for the C and D types), indicating that the
C. botulinum
acquired the toxin genes quite far in the evolutionary past. Nevertheless, further transfers still happen via the plasmids and other mobile elements the genes are located on.
[17]
Toxin types in disease
[
edit
]
Only
botulinum toxin
types A, B, E, F and H (FA) cause disease in humans. Types A, B, and E are associated with food-borne illness, while type E is specifically associated with fish products. Type C produces limber-neck in birds and type D causes botulism in other mammals.
[18]
No disease is associated with type G.
[19]
The "gold standard" for determining toxin type is a mouse bioassay, but the genes for types A, B, E, and F can now be readily differentiated using
quantitative PCR
.
[20]
Type "H" is in fact a recombinant toxin from types A and F. It can be neutralized by type A antitoxin and no longer is considered a distinct type.
[21]
A few strains from organisms genetically identified as other
Clostridium
species have caused human botulism:
C. butyricum
has produced type E toxin
[22]
and
C. baratii
had produced type F toxin.
[23]
The ability of
C. botulinum
to naturally transfer neurotoxin genes to other clostridia is concerning, especially in the
food industry
, where preservation systems are designed to destroy or inhibit only
C. botulinum
but not other
Clostridium
species.
[12]
Metabolism
[
edit
]
Many
C. botulinum
genes play a role in the breakdown of essential carbohydrates and the metabolism of sugars. Chitin is the preferred source of carbon and nitrogen for
C. botulinum
.
[24]
Hall A strain of
C. botulinum
has an active chitinolytic system to aid in the breakdown of chitin.
[24]
Type A and B of
C. botulinum
production of BoNT is affected by nitrogen and carbon nutrition.
[25]
[26]
[27]
There is evidence that these processes are also under catabolite repression.
[28]
Groups
[
edit
]
Physiological differences and genome sequencing at 16S
rRNA
level support the subdivision of the
C. botulinum
species into groups I-IV.
[10]
Some authors have briefly used groups V and VI, corresponding to toxin-producing
C. baratii
and
C. butyricum
. What used to be group IV is now
C. argentinense
.
[29]
Phenotypic groups of toxin-producing
Clostridium
[11]
[29]
Property
|
Group I
|
Group II
|
Group III
|
C. argentinense
|
C. baratii
|
C. butyricum
|
Proteolysis (casein)
|
+
|
-
|
-
|
+
|
-
|
-
|
Saccharolysis
|
-
|
+
|
-
|
-
|
Lipase
|
+
|
+
|
+
|
-
|
-
|
-
|
Toxin Types
|
A, B, F
|
B, E, F
|
C, D
|
G
|
F
|
E
|
Toxin gene
|
chromosome/plasmid
|
chromosome/plasmid
|
bacteriophage
|
plasmid
|
chromosome
[30]
|
chromosome
[31]
|
Close relatives
|
|
- C. beijerinckii
- C. butyricum
|
|
N/A (already a species)
|
Although group II cannot degrade native protein such as
casein
, coagulated
egg white
, and cooked meat particles, it is able to degrade
gelatin
.
[32]
Human
botulism
is predominantly caused by group I or II
C. botulinum
.
[32]
Group III organisms mainly cause diseases in non-human animals.
[32]
Laboratory isolation
[
edit
]
In the laboratory,
C. botulinum
is usually isolated in tryptose sulfite
cycloserine
(TSC) growth medium in an anaerobic environment with less than 2% oxygen. This can be achieved by several
commercial kits
that use a chemical reaction to replace O
2
with CO
2
.
C. botulinum
(groups I through III) is a
lipase
-positive microorganism that grows between
pH
of 4.8 and 7.0 and cannot use
lactose
as a primary carbon source, characteristics important for biochemical identification.
[33]
Transmission and sporulation
[
edit
]
The exact mechanism behind
sporulation
of
C. botulinum
is not known. Different strains of
C. botulinum
can be divided into three different groups, group I, II, and III, based on environmental conditions like heat resistance, temperature, and biome.
[34]
Within each group, different strains will use different strategies to adapt to their environment to survive.
[34]
Unlike other clostridial species,
C. botulinum
spores will sporulate as it enters the stationary phase.
[35]
C. botulinum
relies on
quorum-sensing
to initiate the sporulation process.
[35]
C. botulinum
spores are not found in human feces unless the individual has contracted botulism,
[36]
but
C. botulinum
cannot spread from person to person.
[37]
Motility structures
[
edit
]
The most common motility structure for
C. botulinum
is a flagellum. Though this structure is not found in all strains of
C. botulinum
, most produce
peritrichous
flagella.
[38]
When comparing the different strains, there is also differences in the length of the flagella and how many are present on the cell.
[38]
Growth conditions and prevention
[
edit
]
C. botulinum
is a soil bacterium. The spores can survive in most environments and are very hard to kill. They can survive the temperature of boiling water at sea level, thus many foods are canned with a pressurized boil that achieves even higher temperatures, sufficient to kill the spores.
[39]
[40]
This bacteria is widely distributed in nature and can be assumed to be present on all food surfaces. Its optimum growth temperature is within the
mesophilic
range. In spore form, it is a heat resistant pathogen that can survive in low acid foods and grow to produce toxins. The toxin attacks the nervous system and will kill an adult at a dose of around 75 ng.
[41]
This toxin is detoxified by holding food at 100 °C for 10 minutes.
[42]
Botulism poisoning can occur due to preserved or home-canned, low-acid food that was not processed using correct preservation times and/or pressure.
[43]
Growth of the bacterium can be prevented by high
acidity
, high ratio of dissolved
sugar
, high levels of oxygen, very low levels of moisture, or storage at temperatures below 3 °C (38 °F) for type A. For example, in a low-acid, canned vegetable such as
green beans
that are not heated enough to kill the spores (i.e., a pressurized environment) may provide an oxygen-free medium for the spores to grow and produce the toxin. However, pickles are sufficiently acidic to prevent growth;
[44]
even if the spores are present, they pose no danger to the consumer.
Honey
,
corn syrup
, and other sweeteners may contain spores, but the spores cannot grow in a highly concentrated sugar solution; however, when a sweetener is diluted in the low-oxygen, low-acid digestive system of an infant, the spores can grow and produce toxin. As soon as infants begin eating solid food, the digestive juices become too acidic for the bacterium to grow.
[45]
The control of food-borne botulism caused by
C. botulinum
is based almost entirely on thermal destruction (heating) of the spores or inhibiting spore germination into bacteria and allowing cells to grow and produce toxins in foods. Conditions conducive of growth are dependent on various
environmental factors
.
Growth of
C. botulinum
is a risk in low acid foods as defined by having a pH above 4.6
[46]
although growth is significantly retarded for pH below 4.9.
[47]
Taxonomic history
[
edit
]
C. botulinum
was first recognized and isolated in 1895 by
Emile van Ermengem
from home-cured
ham
implicated in a botulism outbreak.
[48]
The isolate was originally named
Bacillus botulinus
, after the Latin word for sausage,
botulus
. ("Sausage poisoning" was a common problem in 18th- and 19th-century Germany, and was most likely caused by botulism.)
[49]
However, isolates from subsequent outbreaks were always found to be
anaerobic
spore formers, so
Ida A. Bengtson
proposed that both be placed into the genus
Clostridium
, as the genus
Bacillus
was restricted to
aerobic
spore-forming rods.
[50]
Since 1959, all species producing the botulinum neurotoxins (types A?G) have been designated
C. botulinum
. Substantial phenotypic and
genotypic
evidence exists to demonstrate
heterogeneity
within the
species
, with at least four clearly-defined "groups" (see
§ Groups
) straddling other species, implying that they each deserve to be a genospecies.
[51]
[29]
The situation as of 2018 is as follows:
[29]
- C. botulinum
type G (= group IV) strains are since 1988 their own species,
C. argentinense
.
[52]
- Group I
C. botulinum
strains that do not produce a botulin toxin are referred to as
C. sporogenes
. Both names are
conserved names
since 1999.
[53]
Group I also contains
C. combesii
.
[54]
- All other botulinum toxin-producing bacteria, not otherwise classified as
C. baratii
or
C. butyricum
,
[55]
is called
C. botulinum
. This group still contains three genogroups.
[29]
Smith
et al.
(2018) argues that group I should be called
C. parabotulinum
and group III be called
C. novyi
sensu lato
, leaving only group II in
C. botulinum
. This argument is not accepted by the
LPSN
and would cause an unjustified change of the
type strain
under the
Prokaryotic Code
.
[29]
Dobritsa
et al.
(2018) argues, without formal descriptions, that group II can potentially be made into two new species.
[11]
The complete genome of
C. botulinum
ATCC 3502 has been sequenced at
Wellcome Trust Sanger Institute
in 2007. This strain encodes a type "A" toxin.
[56]
Diagnosis
[
edit
]
Physicians may consider the diagnosis of botulism based on a patient's clinical presentation, which classically includes an acute onset of bilateral cranial neuropathies and symmetric descending weakness.
[57]
[58]
Other key features of botulism include an absence of fever, symmetric neurologic deficits, normal or slow heart rate and normal blood pressure, and no sensory deficits except for blurred vision.
[59]
[60]
A careful history and physical examination is paramount to diagnose the type of botulism, as well as to rule out other conditions with similar findings, such as
Guillain?Barre syndrome
,
stroke
, and
myasthenia gravis
.
[61]
Depending on the type of botulism considered, different tests for diagnosis may be indicated.
- Foodborne botulism:
serum analysis for toxins by bioassay in mice should be done, as the demonstration of the toxins is diagnostic.
[62]
- Wound botulism:
isolation of
C. botulinum
from the wound site should be attempted, as growth of the bacteria is diagnostic.
[63]
- Adult enteric and infant botulism:
isolation and growth of
C. botulinum
from stool samples is diagnostic.
[64]
Infant botulism is a diagnosis which is often missed in the emergency room.
[65]
Other tests that may be helpful in ruling out other conditions are:
Pathology
[
edit
]
Foodborne botulism
[
edit
]
Signs and symptoms of foodborne botulism typically begin between 18 and 36 hours after the toxin gets into your body, but can range from a few hours to several days, depending on the amount of toxin ingested. Symptoms include:
[69]
[70]
- Double vision
- Blurred vision
- Ptosis
- Nausea, vomiting, and abdominal cramps
- Slurred speech
- Trouble breathing
- Difficulty in swallowing
- Dry mouth
- Muscle weakness
- Constipation
- Reduced or absent deep tendon reactions, such as in the knee
Wound botulism
[
edit
]
Most people who develop wound botulism inject drugs several times a day, so determining a timeline of when onset symptoms first occurred and when the toxin entered the body can be difficult. It is more common in people who inject black tar heroin.
[71]
Wound botulism signs and symptoms include:
[70]
[72]
- Difficulty swallowing or speaking
- Facial weakness on both sides of the face
- Blurred or double vision
- Ptosis
- Trouble breathing
- Paralysis
Infant botulism
[
edit
]
If infant botulism is related to food, such as honey, problems generally begin within 18 to 36 hours after the toxin enters the baby's body. Signs and symptoms include:
[65]
[70]
- Constipation (often the first sign)
- Floppy movements due to muscle weakness and trouble controlling the head
- Weak cry
- Irritability
- Drooling
- Ptosis
- Tiredness
- Difficulty sucking or feeding
- Paralysis
[70]
Beneficial effects of botulinum toxin
[
edit
]
Purified botulinum toxin is diluted by a physician for treatment of:
[73]
- Congenital pelvic tilt
- Spasmodic dysphasia (the inability of the muscles of the larynx)
- Achalasia (esophageal stricture)
- Strabismus (crossed eyes)
- Paralysis of the facial muscles
- Failure of the cervix
- Blinking frequently
- Anti-cancer drug delivery
[74]
Adult intestinal toxemia
[
edit
]
A very rare form of botulism that occurs by the same route as infant botulism but is among adults. Occurs rarely and sporadically. Signs and symptoms include:
[75]
- Abdominal pain
- Blurred vision
- Diarrhea
- Dysarthria
- Imbalance
- Weakness in arms and hand area
[76]
Treatment
[
edit
]
In the case of a diagnosis or suspicion of botulism, patients should be hospitalized immediately, even if the diagnosis and/or tests are pending. Additionally if botulism is suspected, patients should be treated immediately with antitoxin therapy in order to reduce mortality. Immediate intubation is also highly recommended, as respiratory failure is the primary cause of death from botulism.
[77]
[78]
[79]
In North America, an equine-derived heptavalent botulinum antitoxin is used to treat all serotypes of non-infant naturally occurring botulism. For infants less than one year of age, botulism immune globulin is used to treat type A or type B.
[80]
[81]
Outcomes vary between one and three months, but with prompt interventions, mortality from botulism ranges from less than 5 percent to 8 percent.
[82]
Vaccination
[
edit
]
There used to be a formalin-treated
toxoid
vaccine against botulism (serotypes A-E), but it was discontinued in 2011 due to declining potency in the toxoid stock. It was originally intended for people at risk of exposure. A few new vaccines are under development.
[83]
Use and detection
[
edit
]
C. botulinum
is used to prepare the medicaments
Botox
,
Dysport
,
Xeomin
, and
Neurobloc
used to selectively paralyze muscles to temporarily relieve muscle function. It has other "
off-label
" medical purposes, such as treating severe facial pain, such as that caused by
trigeminal neuralgia
.
[84]
Botulinum toxin
produced by
C. botulinum
is often believed to be a potential
bioweapon
as it is so potent that it takes about 75
nanograms
to kill a person (
LD
50
of 1 ng/kg,
[41]
assuming an average person weighs ~75 kg); 1 kilogram of it would be enough to kill the
entire human population
.
A "mouse protection" or "mouse bioassay" test determines the type of
C. botulinum
toxin present using
monoclonal antibodies
. An enzyme-linked immunosorbent assay (
ELISA
) with
digoxigenin
-labeled antibodies can also be used to detect the toxin,
[85]
and
quantitative PCR
can detect the toxin genes in the organism.
[20]
C. botulinum
in different geographical locations
[
edit
]
A number of
quantitative
surveys
for
C. botulinum
spores
in the environment have suggested a prevalence of specific toxin types in given geographic areas, which remain unexplained.
Location
|
|
North America
|
Type A
C. botulinum
predominates the
soil
samples from the western regions, while type B is the major type found in eastern areas.
[86]
The type-B organisms were of the proteolytic type I.
Sediments
from the
Great Lakes
region were surveyed after outbreaks of botulism among commercially reared
fish
, and only type E spores were detected.
[87]
[88]
[89]
In a survey, type-A strains were isolated from soils that were
neutral
to
alkaline
(average pH 7.5), while type-B strains were isolated from slightly
acidic
soils (average pH 6.23).
|
Europe
|
C. botulinum
type E is prevalent in aquatic sediments in Norway and Sweden,
[90]
Denmark,
[91]
</ref> the Netherlands, the Baltic coast of Poland, and Russia.
[86]
The type-E
C. botulinum
was suggested to be a true
aquatic
organism, which was indicated by the correlation between the level of type-E contamination and flooding of the land with seawater. As the land dried, the level of type E decreased and type B became dominant
[92]
In soil and sediment from the United Kingdom,
C. botulinum
type B predominates. In general, the incidence is usually lower in soil than in
sediment
. In Italy, a survey conducted in the vicinity of
Rome
found a low level of contamination; all strains were proteolytic
C. botulinum
types A or B.
[93]
|
Australia
|
C. botulinum
type A was found to be present in soil samples from mountain areas of
Victoria
.
[94]
Type-B organisms were detected in marine mud from
Tasmania
.
[95]
Type-A
C. botulinum
has been found in
Sydney
suburbs and types A and B were isolated from
urban
areas. In a well-defined area of the Darling-Downs region of
Queensland
, a study showed the prevalence and persistence of
C. botulinum
type B after many cases of botulism in
horses
.
|
References
[
edit
]
- ^
a
b
Tiwari A, Nagalli S (2021).
"Clostridium Botulinum"
.
StatPearls
. Treasure Island (FL): StatPearls Publishing.
PMID
31971722
. Retrieved
2021-09-23
.
- ^
a
b
c
Peck MW (2009). "Biology and genomic analysis of Clostridium botulinum".
Advances in Microbial Physiology
.
55
: 183?265, 320.
doi
:
10.1016/S0065-2911(09)05503-9
.
ISBN
978-0-12-374790-7
.
PMID
19573697
.
- ^
a
b
Lindstrom M, Korkeala H (April 2006).
"Laboratory diagnostics of botulism"
.
Clinical Microbiology Reviews
.
19
(2): 298?314.
doi
:
10.1128/cmr.19.2.298-314.2006
.
PMC
1471988
.
PMID
16614251
.
- ^
Ko?enina S, Masuyer G, Zhang S, Dong M, Stenmark P (June 2019).
"Crystal structure of the catalytic domain of the Weissella oryzae botulinum-like toxin"
.
FEBS Letters
.
593
(12): 1403?1410.
doi
:
10.1002/1873-3468.13446
.
PMID
31111466
.
- ^
a
b
(2010). Chapter 19.
Clostridium
,
Peptostreptococcus
,
Bacteroides
, and Other Anaerobes. In Ryan K.J., Ray C (Eds),
Sherris Medical Microbiology
, 5th ed.
ISBN
978-0-07-160402-4
- ^
Schneider KR, Silverberg R, Chang A, Goodrich Schneider RM (9 January 2015).
"Preventing Foodborne Illness:
Clostridium botulinum
"
.
edis.ifas.ufl.edu
. University of Florida IFAS Extension
. Retrieved
7 February
2017
.
- ^
Doyle MP (2007).
Food Microbiology: Fundamentals and Frontiers
. ASM Press.
ISBN
978-1-55581-208-9
.
- ^
Peck MW, Stringer SC, Carter AT (April 2011). "Clostridium botulinum in the post-genomic era".
Food Microbiology
.
28
(2): 183?191.
doi
:
10.1016/j.fm.2010.03.005
.
PMID
21315972
.
- ^
Shukla HD, Sharma SK (2005). "Clostridium botulinum: a bug with beauty and weapon".
Critical Reviews in Microbiology
.
31
(1): 11?18.
doi
:
10.1080/10408410590912952
.
PMID
15839401
.
S2CID
2855356
.
- ^
a
b
Austin JW (January 1, 2003).
"Clostridium | Occurrence of Clostridium botulinum"
.
Clostridium
. Academic Press. pp. 1407?1413.
doi
:
10.1016/B0-12-227055-X/00255-8
.
ISBN
978-0-12-227055-0
. Retrieved
February 19,
2021
.
- ^
a
b
c
Dobritsa AP, Kutumbaka KK, Samadpour M (September 2018).
"Reclassification of Eubacterium combesii and discrepancies in the nomenclature of botulinum neurotoxin-producing clostridia: Challenging Opinion 69. Request for an Opinion"
.
International Journal of Systematic and Evolutionary Microbiology
.
68
(9): 3068?3075.
doi
:
10.1099/ijsem.0.002942
.
PMID
30058996
.
- ^
a
b
c
Hill KK, Smith TJ (2012). "Genetic Diversity Within Clostridium botulinum Serotypes, Botulinum Neurotoxin Gene Clusters and Toxin Subtypes".
Botulinum Neurotoxins
. Current Topics in Microbiology and Immunology. Vol. 364. pp. 1?20.
doi
:
10.1007/978-3-642-33570-9_1
.
ISBN
978-3-642-33569-3
.
PMID
23239346
.
- ^
Peck MW, Smith TJ, Anniballi F, Austin JW, Bano L, Bradshaw M, et al. (January 2017).
"Historical Perspectives and Guidelines for Botulinum Neurotoxin Subtype Nomenclature"
.
Toxins
.
9
(1): 38.
doi
:
10.3390/toxins9010038
.
PMC
5308270
.
PMID
28106761
.
- ^
Notermans S, Havellar AH (1980). "Removal and inactivation of botulinum toxin during production of drinking water from surface water".
Antonie van Leeuwenhoek
.
46
(5): 511?514.
doi
:
10.1007/BF00395840
.
S2CID
21102990
.
- ^
Montecucco C, Molgo J (June 2005). "Botulinal neurotoxins: revival of an old killer".
Current Opinion in Pharmacology
.
5
(3): 274?279.
doi
:
10.1016/j.coph.2004.12.006
.
PMID
15907915
.
- ^
Hatheway CL, McCroskey LM (December 1987).
"Examination of feces and serum for diagnosis of infant botulism in 336 patients"
.
Journal of Clinical Microbiology
.
25
(12): 2334?2338.
doi
:
10.1128/JCM.25.12.2334-2338.1987
.
PMC
269483
.
PMID
3323228
.
- ^
Poulain B, Popoff MR (January 2019).
"Why Are Botulinum Neurotoxin-Producing Bacteria So Diverse and Botulinum Neurotoxins So Toxic?"
.
Toxins
.
11
(1): 34.
doi
:
10.3390/toxins11010034
.
PMC
6357194
.
PMID
30641949
.
- ^
Meurens F, Carlin F, Federighi M, Filippitzi ME, Fournier M, Fravalo P, et al. (2023-01-05).
"
Clostridium botulinum
type C, D, C/D, and D/C: An update"
.
Frontiers in Microbiology
.
13
: 1099184.
doi
:
10.3389/fmicb.2022.1099184
.
PMC
9849819
.
PMID
36687640
.
- ^
(2013). Chapter 11. Spore-Forming Gram-Positive Bacilli:
Bacillus
and
Clostridium
Species. In Brooks G.F., Carroll K.C., Butel J.S., Morse S.A., Mietzner T.A. (Eds),
Jawetz, Melnick, & Adelberg's Medical Microbiology
, 26th ed.
ISBN
978-0-07-179031-4
- ^
a
b
Satterfield BA, Stewart AF, Lew CS, Pickett DO, Cohen MN, Moore EA, et al. (January 2010).
"A quadruplex real-time PCR assay for rapid detection and differentiation of the Clostridium botulinum toxin genes A, B, E and F"
.
Journal of Medical Microbiology
.
59
(Pt 1): 55?64.
doi
:
10.1099/jmm.0.012567-0
.
PMID
19779029
.
- ^
Maslanka SE, Luquez C, Dykes JK, Tepp WH, Pier CL, Pellett S, et al. (February 2016).
"A Novel Botulinum Neurotoxin, Previously Reported as Serotype H, Has a Hybrid-Like Structure With Regions of Similarity to the Structures of Serotypes A and F and Is Neutralized With Serotype A Antitoxin"
.
The Journal of Infectious Diseases
.
213
(3): 379?385.
doi
:
10.1093/infdis/jiv327
.
PMC
4704661
.
PMID
26068781
.
- ^
Aureli P, Fenicia L, Pasolini B, Gianfranceschi M, McCroskey LM, Hatheway CL (August 1986). "Two cases of type E infant botulism caused by neurotoxigenic Clostridium butyricum in Italy".
The Journal of Infectious Diseases
.
154
(2): 207?211.
doi
:
10.1093/infdis/154.2.207
.
PMID
3722863
.
- ^
Hall JD, McCroskey LM, Pincomb BJ, Hatheway CL (April 1985).
"Isolation of an organism resembling Clostridium barati which produces type F botulinal toxin from an infant with botulism"
.
Journal of Clinical Microbiology
.
21
(4): 654?655.
doi
:
10.1128/JCM.21.4.654-655.1985
.
PMC
271744
.
PMID
3988908
.
- ^
a
b
Sebaihia M, Peck MW, Minton NP, Thomson NR, Holden MT, Mitchell WJ, et al. (July 2007).
"Genome sequence of a proteolytic (Group I) Clostridium botulinum strain Hall A and comparative analysis of the clostridial genomes"
.
Genome Research
.
17
(7): 1082?1092.
doi
:
10.1101/gr.6282807
.
PMC
1899119
.
PMID
17519437
.
- ^
Leyer GJ, Johnson EA (October 1990). "Repression of toxin production by tryptophan in Clostridium botulinum type E".
Archives of Microbiology
.
154
(5): 443?447.
Bibcode
:
1990ArMic.154..443L
.
doi
:
10.1007/BF00245225
.
PMID
2256780
.
- ^
Patterson-Curtis SI, Johnson EA (June 1989).
"Regulation of neurotoxin and protease formation in Clostridium botulinum Okra B and Hall A by arginine"
.
Applied and Environmental Microbiology
.
55
(6): 1544?1548.
Bibcode
:
1989ApEnM..55.1544P
.
doi
:
10.1128/aem.55.6.1544-1548.1989
.
PMC
202901
.
PMID
2669631
.
- ^
Schantz EJ, Johnson EA (1992).
"Properties and use of botulinum toxin and other microbial neurotoxins in medicine"
.
Microbiological Reviews
.
56
(1): 80?99.
doi
:
10.1128/MMBR.56.1.80-99.1992
.
ISSN
0146-0749
.
PMC
372855
.
PMID
1579114
.
- ^
Johnson EA, Bradshaw M (November 2001). "Clostridium botulinum and its neurotoxins: a metabolic and cellular perspective".
Toxicon
.
39
(11): 1703?1722.
Bibcode
:
2001Txcn...39.1703J
.
doi
:
10.1016/S0041-0101(01)00157-X
.
PMID
11595633
.
- ^
a
b
c
d
e
f
Smith T, Williamson CH, Hill K, Sahl J, Keim P (September 2018).
"Botulinum Neurotoxin-Producing Bacteria. Isn't It Time that We Called a Species a Species?"
.
mBio
.
9
(5).
doi
:
10.1128/mbio.01469-18
.
PMC
6156192
.
PMID
30254123
.
- ^
Mazuet C, Legeay C, Sautereau J, Bouchier C, Criscuolo A, Bouvet P, et al. (February 2017).
"Characterization of Clostridium Baratii Type F Strains Responsible for an Outbreak of Botulism Linked to Beef Meat Consumption in France"
.
PLOS Currents
.
9
.
doi
:
10.1371/currents.outbreaks.6ed2fe754b58a5c42d0c33d586ffc606
(inactive 31 January 2024).
PMC
5959735
.
PMID
29862134
.
{{
cite journal
}}
: CS1 maint: DOI inactive as of January 2024 (
link
)
- ^
Hill KK, Xie G, Foley BT, Smith TJ, Munk AC, Bruce D, et al. (October 2009).
"Recombination and insertion events involving the botulinum neurotoxin complex genes in Clostridium botulinum types A, B, E and F and Clostridium butyricum type E strains"
.
BMC Biology
.
7
(1): 66.
doi
:
10.1186/1741-7007-7-66
.
PMC
2764570
.
PMID
19804621
.
- ^
a
b
c
Carter AT, Peck MW (May 2015).
"Genomes, neurotoxins and biology of Clostridium botulinum Group I and Group II"
.
Research in Microbiology
.
166
(4): 303?317.
doi
:
10.1016/j.resmic.2014.10.010
.
PMC
4430135
.
PMID
25445012
.
- ^
Madigan MT, Martinko JM, eds. (2005).
Brock Biology of Microorganisms
(11th ed.). Prentice Hall.
ISBN
978-0-13-144329-7
.
- ^
a
b
Portinha IM, Douillard FP, Korkeala H, Lindstrom M (January 2022).
"Sporulation Strategies and Potential Role of the Exosporium in Survival and Persistence of
Clostridium botulinum
"
.
International Journal of Molecular Sciences
.
23
(2): 754.
doi
:
10.3390/ijms23020754
.
PMC
8775613
.
PMID
35054941
.
>
- ^
a
b
Shen A, Edwards AN, Sarker MR, Paredes-Sabja D (November 2019). Fischetti VA, Novick RP, Ferretti JJ, Portnoy DA, Braunstein M, Rood JI (eds.).
"Sporulation and Germination in Clostridial Pathogens"
.
Microbiology Spectrum
.
7
(6).
doi
:
10.1128/microbiolspec.GPP3-0017-2018
.
PMC
6927485
.
PMID
31858953
.
- ^
Dowell VR (1977).
"Coproexamination for Botulinal Toxin and Clostridium botulinum"
.
JAMA
.
238
(17): 1829.
doi
:
10.1001/jama.1977.03280180033021
. Retrieved
2024-04-11
.
- ^
"Botulism"
.
www.who.int
. Retrieved
2024-04-16
.
- ^
a
b
Paul CJ, Twine SM, Tam KJ, Mullen JA, Kelly JF, Austin JW, et al. (May 2007).
"Flagellin Diversity in Clostridium botulinum Groups I and II: a New Strategy for Strain Identification"
.
Applied and Environmental Microbiology
.
73
(9): 2963?2975.
Bibcode
:
2007ApEnM..73.2963P
.
doi
:
10.1128/AEM.02623-06
.
ISSN
0099-2240
.
PMC
1892883
.
PMID
17351097
.
- ^
"Prevent Botulism"
.
Centers for Disease Control and Prevention (CDC)
. 2019-06-06
. Retrieved
2023-04-23
.
- ^
"Botulism: take care when canning low-acid foods"
.
extension.umn.edu
. Retrieved
2023-04-23
.
- ^
a
b
Fleming DO.
Biological Safety: principles and practices
. Vol. 2000. ASM Press. p. 267.
- ^
"Chapter 13: Clostridium botulinum Toxin Formation"
(PDF)
.
Fda.gov
.
Archived
(PDF)
from the original on 2021-02-08
. Retrieved
18 March
2022
.
- ^
"Home Canning and Botulism"
.
Centers for Disease Control and Prevention
. Retrieved
14 April
2021
.
- ^
Ito KA, Chen JK, Lerke PA, Seeger ML, Unverferth JA (July 1976).
"Effect of acid and salt concentration in fresh-pack pickles on the growth of Clostridium botulinum spores"
.
Applied and Environmental Microbiology
.
32
(1): 121?124.
Bibcode
:
1976ApEnM..32..121I
.
doi
:
10.1128/aem.32.1.121-124.1976
.
PMC
170016
.
PMID
9898
.
- ^
"Botulism"
.
The Lecturio Medical Concept Library
. Retrieved
5 July
2021
.
- ^
"Guidance for Commercial Processors of Acidified & Low-Acid Canned Foods"
. U.S. Food and Drug Administration
. Retrieved
8 October
2016
.
- ^
Odlaug TE, Pflug IJ (March 1979).
"Clostridium botulinum growth and toxin production in tomato juice containing Aspergillus gracilis"
.
Applied and Environmental Microbiology
.
37
(3): 496?504.
Bibcode
:
1979ApEnM..37..496O
.
doi
:
10.1128/aem.37.3.496-504.1979
.
PMC
243244
.
PMID
36843
.
- ^
van Ergmengem E (1897). "Uber einen neuen anaeroben Bacillus und seine Beziehungen Zum Botulismus".
Zeitschrift fur Hygiene und Infektionskrankheiten
.
26
: 1?8.
- ^
Erbguth FJ (March 2004). "Historical notes on botulism, Clostridium botulinum, botulinum toxin, and the idea of the therapeutic use of the toxin".
Movement Disorders
.
19
(Suppl 8): S2?S6.
doi
:
10.1002/mds.20003
.
PMID
15027048
.
S2CID
8190807
.
- ^
Bengston IA (1924).
"Studies on organisms concerned as causative factors in botulism"
.
Bulletin (Hygienic Laboratory (U.S.))
.
136
: 101 fv.
- ^
Uzal FA, Songer JG, Prescott JF, Popoff MR (21 June 2016). "Taxonomic Relationships among the Clostridia".
Clostridial Diseases of Animals
. pp. 1?5.
doi
:
10.1002/9781118728291.ch1
.
ISBN
978-1-118-72829-1
.
- ^
Suen JC, Hatheway CL, Steigerwalt AG, Brenner DJ (1988).
"
Clostridium argentinense sp.nov.
: a genetically homogeneous group composed of all strains of
Clostridium botulinum
type G and some nonttoxigenic strains previously identified as
Clostridium subterminale
or
Clostridium hastiforme
"
.
International Journal of Systematic Bacteriology
.
38
: 375?381.
doi
:
10.1099/00207713-38-4-375
.
- ^
"Rejection of Clostridium putrificum and conservation of Clostridium botulinum and Clostridium sporogenes-Opinion 69. Judicial Commission of the International Committee on Systematic Bacteriology"
.
International Journal of Systematic Bacteriology
. 49 Pt 1 (1): 339. January 1999.
doi
:
10.1099/00207713-49-1-339
.
PMID
10028279
.
- ^
"Species: Clostridium combesii"
.
lpsn.dsmz.de
.
- ^
Arahal DR, Busse HJ, Bull CT, Christensen H, Chuvochina M, Dedysh SN, et al. (August 2022). "Judicial Opinions 112-122".
International Journal of Systematic and Evolutionary Microbiology
.
72
(8).
doi
:
10.1099/ijsem.0.005481
.
PMID
35947640
.
S2CID
251470203
.
- ^
"Clostridium botulinum A str. ATCC 3502 genome assembly ASM6358v1"
.
NCBI
.
- ^
Cherington M (June 1998). "Clinical spectrum of botulism".
Muscle & Nerve
.
21
(6): 701?710.
doi
:
10.1002/(sici)1097-4598(199806)21:6<701::aid-mus1>3.0.co;2-b
.
PMID
9585323
.
- ^
Cai S, Singh BR, Sharma S (April 2007). "Botulism diagnostics: from clinical symptoms to in vitro assays".
Critical Reviews in Microbiology
.
33
(2): 109?125.
doi
:
10.1080/10408410701364562
.
PMID
17558660
.
S2CID
23470999
.
- ^
"Diagnosis and Treatment | Botulism"
. CDC
. Retrieved
2017-10-08
.
- ^
"Botulism: Rare but serious food poisoning"
. Mayo Clinic
. Retrieved
2017-11-18
.
- ^
Rao AK, Sobel J, Chatham-Stephens K, Luquez C (May 2021).
"Clinical Guidelines for Diagnosis and Treatment of Botulism, 2021"
.
MMWR. Recommendations and Reports
.
70
(2): 1?30.
doi
:
10.15585/mmwr.rr7002a1
.
PMC
8112830
.
PMID
33956777
.
- ^
Lindstrom M, Korkeala H (April 2006).
"Laboratory diagnostics of botulism"
.
Clinical Microbiology Reviews
.
19
(2): 298?314.
doi
:
10.1128/CMR.19.2.298-314.2006
.
PMC
1471988
.
PMID
16614251
.
- ^
Akbulut D, Grant KA, McLauchlin J (September 2005).
"Improvement in laboratory diagnosis of wound botulism and tetanus among injecting illicit-drug users by use of real-time PCR assays for neurotoxin gene fragments"
.
Journal of Clinical Microbiology
.
43
(9): 4342?4348.
doi
:
10.1128/JCM.43.9.4342-4348.2005
.
PMC
1234055
.
PMID
16145075
.
- ^
Dezfulian M, McCroskey LM, Hatheway CL, Dowell VR (March 1981).
"Selective medium for isolation of Clostridium botulinum from human feces"
.
Journal of Clinical Microbiology
.
13
(3): 526?531.
doi
:
10.1128/JCM.13.3.526-531.1981
.
PMC
273826
.
PMID
7016901
.
- ^
a
b
Antonucci L, Locci C, Schettini L, Clemente MG, Antonucci R (September 2021). "Infant botulism: an underestimated threat".
Infectious Diseases
.
53
(9): 647?660.
doi
:
10.1080/23744235.2021.1919753
.
PMID
33966588
.
- ^
O'Suilleabhain P, Low PA, Lennon VA (January 1998). "Autonomic dysfunction in the Lambert-Eaton myasthenic syndrome: serologic and clinical correlates".
Neurology
.
50
(1): 88?93.
doi
:
10.1212/wnl.50.1.88
.
PMID
9443463
.
S2CID
39437882
.
- ^
Mechem CC, Walter FG (June 1994).
"Wound botulism"
.
Veterinary and Human Toxicology
.
36
(3): 233?237.
PMID
8066973
.
- ^
Taraschenko OD, Powers KM (June 2014). "Neurotoxin-induced paralysis: a case of tick paralysis in a 2-year-old child".
Pediatric Neurology
.
50
(6): 605?607.
doi
:
10.1016/j.pediatrneurol.2014.01.041
.
PMID
24679414
.
- ^
Lonati D, Schicchi A, Crevani M, Buscaglia E, Scaravaggi G, Maida F, et al. (August 2020).
"Foodborne Botulism: Clinical Diagnosis and Medical Treatment"
.
Toxins
.
12
(8): 509.
doi
:
10.3390/toxins12080509
.
PMC
7472133
.
PMID
32784744
.
- ^
a
b
c
d
"Botulism Symptoms"
.
Mayo Clinic
. June 13, 2015
. Retrieved
January 25,
2016
.
- ^
"Injection Drug Use and Wound Botulism | Botulism | CDC"
.
www.cdc.gov
. 2022-05-31
. Retrieved
2024-04-17
.
- ^
Schulte M, Hamsen U, Schildhauer TA, Ramczykowski T (October 2017).
"Effective and rapid treatment of wound botulism, a case report"
.
BMC Surgery
.
17
(1): 103.
doi
:
10.1186/s12893-017-0300-4
.
PMC
5658925
.
PMID
29073888
.
- ^
Chiu SY, Patel B, Burns MR, Legacy J, Shukla AW, Ramirez-Zamora A, et al. (2020-02-27).
"High-dose Botulinum Toxin Therapy: Safety, Benefit, and Endurance of Efficacy"
.
Tremor and Other Hyperkinetic Movements
.
10
.
doi
:
10.5334/tohm.527
.
ISSN
2160-8288
.
- ^
Arnon SS, Schechter R, Inglesby TV, Henderson DA, Bartlett JG, Ascher MS, et al. (February 2001). "Botulinum toxin as a biological weapon: medical and public health management".
JAMA
.
285
(8): 1059?1070.
doi
:
10.1001/jama.285.8.1059
.
PMID
11209178
.
- ^
Harris RA, Anniballi F, Austin JW (January 2020).
"Adult Intestinal Toxemia Botulism"
.
Toxins
.
12
(2): 81.
doi
:
10.3390/toxins12020081
.
PMC
7076759
.
PMID
31991691
.
- ^
"Botulism"
.
Centers for Disease Control and Prevention
. Retrieved
23 October
2016
.
- ^
Witoonpanich R, Vichayanrat E, Tantisiriwit K, Wongtanate M, Sucharitchan N, Oranrigsupak P, et al. (March 2010). "Survival analysis for respiratory failure in patients with food-borne botulism".
Clinical Toxicology
.
48
(3): 177?183.
doi
:
10.3109/15563651003596113
.
PMID
20184431
.
S2CID
23108891
.
- ^
Sandrock CE, Murin S (August 2001). "Clinical predictors of respiratory failure and long-term outcome in black tar heroin-associated wound botulism".
Chest
.
120
(2): 562?566.
doi
:
10.1378/chest.120.2.562
.
PMID
11502659
.
- ^
Wongtanate M, Sucharitchan N, Tantisiriwit K, Oranrigsupak P, Chuesuwan A, Toykeaw S, et al. (August 2007).
"Signs and symptoms predictive of respiratory failure in patients with foodborne botulism in Thailand"
.
The American Journal of Tropical Medicine and Hygiene
.
77
(2): 386?389.
doi
:
10.4269/ajtmh.2007.77.386
.
PMID
17690419
.
- ^
"Botulism - Guide for Healthcare Professionals"
.
Health Canada
. 2012-07-18
. Retrieved
2023-11-01
.
- ^
"Investigational Heptavalent Botulinum Antitoxin (HBAT) to Replace Licensed Botulinum Antitoxin AB and Investigational Botulinum Antitoxin E"
.
www.cdc.gov
. Retrieved
2023-11-01
.
- ^
Varma JK, Katsitadze G, Moiscrafishvili M, Zardiashvili T, Chokheli M, Tarkhashvili N, et al. (August 2004). "Signs and symptoms predictive of death in patients with foodborne botulism--Republic of Georgia, 1980-2002".
Clinical Infectious Diseases
.
39
(3): 357?362.
doi
:
10.1086/422318
.
PMID
15307002
.
S2CID
20675701
.
- ^
Sundeen G, Barbieri JT (September 2017).
"Vaccines against Botulism"
.
Toxins
.
9
(9): 268.
doi
:
10.3390/toxins9090268
.
PMC
5618201
.
PMID
28869493
.
- ^
Guardiani E, Sadoughi B, Blitzer A, Sirois D (February 2014). "A new treatment paradigm for trigeminal neuralgia using Botulinum toxin type A".
The Laryngoscope
.
124
(2): 413?417.
doi
:
10.1002/lary.24286
.
PMID
23818108
.
- ^
Sharma SK, Ferreira JL, Eblen BS, Whiting RC (February 2006).
"Detection of type A, B, E, and F Clostridium botulinum neurotoxins in foods by using an amplified enzyme-linked immunosorbent assay with digoxigenin-labeled antibodies"
.
Applied and Environmental Microbiology
.
72
(2): 1231?1238.
Bibcode
:
2006ApEnM..72.1231S
.
doi
:
10.1128/AEM.72.2.1231-1238.2006
.
PMC
1392902
.
PMID
16461671
.
- ^
a
b
Hauschild AH (1989). "Clostridium botulinum.". In Doyle MP (ed.).
Food-borne Bacterial Pathogens
. New York: Marcel Dekker. pp. 111?189.
- ^
Bott TL, Johnson J, Foster EM, Sugiyama H (May 1968).
"Possible origin of the high incidence of Clostridium botulinum type E in an inland bay (Green Bay of Lake Michigan)"
.
Journal of Bacteriology
.
95
(5): 1542?7.
doi
:
10.1128/jb.95.5.1542-1547.1968
.
PMC
252172
.
PMID
4870273
.
- ^
Eklund MW, Peterson ME, Poysky FT, Peck LW, Conrad JF (February 1982). "Botulism in juvenile coho salmon (Oncorhynchus kisutch) in the United States".
Aquaculture
.
27
(1): 1?11.
Bibcode
:
1982Aquac..27....1E
.
doi
:
10.1016/0044-8486(82)90104-1
.
- ^
Eklund MW, Poysky FT, Peterson ME, Peck LW, Brunson WD (October 1984). "Type E botulism in salmonids and conditions contributing to outbreaks".
Aquaculture
.
41
(4): 293?309.
Bibcode
:
1984Aquac..41..293E
.
doi
:
10.1016/0044-8486(84)90198-4
.
- ^
Johannsen A (April 1963). "Clostridium botulinum in Sweden and the adjacent waters".
Journal of Applied Bacteriology
.
26
(1): 43?47.
doi
:
10.1111/j.1365-2672.1963.tb01153.x
.
- ^
Huss HH (April 1980).
"Distribution of Clostridium botulinum"
.
Applied and Environmental Microbiology
.
39
(4): 764?9.
Bibcode
:
1980ApEnM..39..764H
.
doi
:
10.1128/aem.39.4.764-769.1980
.
PMC
291416
.
PMID
6990867
.
- ^
Portinha IM, Douillard FP, Korkeala H, Lindstrom M (January 2022).
"Sporulation Strategies and Potential Role of the Exosporium in Survival and Persistence of
Clostridium botulinum
"
.
International Journal of Molecular Sciences
.
23
(2): 754.
doi
:
10.3390/ijms23020754
.
PMC
8775613
.
PMID
35054941
.
- ^
Creti R, Fenicia J, Aureli P (May 1990). "Occurrence of Clostridium botulinum in the soil of the vicinity of Rome".
Current Microbiology
.
20
(5): 317?321.
doi
:
10.1007/bf02091912
.
- ^
Eales CE, Gillespie JM (August 1947). "The isolation of Clostridium botulinum type A from Victorian soils".
The Australian Journal of Science
.
10
(1): 20.
PMID
20267540
.
- ^
Ohye DF, Scott WJ (1957).
"Studies in the physiology of
Clostridium botulinum
type E"
.
Australian Journal of Biological Sciences
.
10
: 85?94.
doi
:
10.1071/BI9570085
.
Further reading
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