Foodborne Botulism or…
Please don’t pass the olives! Unusual
cases of food poisoning.
Corinne Amar PhD
Head of the foodborne pathogens reference services FPRS,
Gastrointestinal Bacteria Reference Unit GBRU
Botulism
• Rare but potentially fatal disease that causes paralysis
• Caused by neurotoxins of Clostridium botulinum and by rare
strains of C. baratii and C. butyricum.
• Botulism affect humans and other animals
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Foodborne botulism
A bit of history
• Botulism first recorded in Europe in 1735 and that was suspected of being
associated with a German sausage. It was named after the Latin word for
sausage, ''botulus’’
• 1817: first publication of outbreak reports
• In 1895, a botulism outbreak (34 cases) after a funeral dinner with smoked
ham in the small Belgian village of Ellezelles led to the isolation of the
pathogen Clostridium botulinum by Emile Pierre van Ermengem,
bacteriologist at the University of Ghent.
Johann von Autenrieth
1752-1832
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Foodborne botulism
Emile Pierre van Ermengem
1851 – 1922 or 1932
The Hotel Loch Maree tragedy
First recorded outbreak of botulism in the UK.
Summer 1922: a group of Londoners, staying at the hotel ordered their meal
to be prepared in advance.
Potted duck had been on the menu all summer and on the 14th August, the
last of the duck meat from the glass jar was scrapped to make sandwiches
which were wrapped for a picnic.
All 8 people ate the sandwiches.
By following morning they were all ill.
72h later, 6 people were dead and the
other 2 died within the next 5 days.
Bruce White from University of Bristol isolated
Clostridium ‘botulinus’ from remainder of one sandwich.
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Foodborne botulism
Clostridium botulinum
Organism exists in the natural environment as resistant spores in soil,
sediment, mud, water.
Under the right conditions (anaerobic) spores germinate, multiply and
produce toxin
Botulism Neurotoxin or BoNT can also be produced by rare strains of C.
butyricum and C. baratii
• Gram positive rod
• Strictly anaerobe
• Six antigenically distinct neurotoxins A to G
• Types A, B, E and F associated with human disease,
• Types C and D animal disease, G no disease
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Foodborne botulism
Four distinct groups of organisms by phenotypic characteristics and DNA
homology –human disease groups I, II
Group I
Group II
(proteolytic activity)
(non proteolytic)
A, B, F
B, E, F
Minimum growth temperature
10
3.3
Optimum growth temperature
35-40
18-25
D 100ºC (spores)
25 minutes
<0.1 minutes
D 121ºC (spores)
0.1-0.2 minutes
<0.001 minutes
Minimum pH for growth
4.6
5
[Inhibitory salt] (%)
10
5
Toxin types
6
Foodborne botulism
Forms of botulism:
• Foodborne botulism
• Infant botulism
(main form of botulism at present in the UK)
• Wound botulism
• Accidental or deliberate release
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Foodborne botulism
Foodborne botulism
• Intoxication
• by ingestion of preformed toxin in food where the organism
has grown
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Foodborne botulism
Infant botulism
• Toxico infection
• By ingestion of spores which germinate, multiply and
produce toxin in the gut: gut colonisation by the organism
• Usually occurs in infants <1 year
9
Foodborne botulism
Wound botulism
Wound infection where the bacterium multiplies under
anaerobic conditions and produces toxin
Exclusive to illegal injection of drugs in the UK but reported in
other patient groups elsewhere
10
Foodborne botulism
Accidental/ deliberate release
•Cosmetic or therapeutic
•Bioterrorism – C. botulinum is a schedule 5 organism
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Foodborne botulism
Mechanism of action of the botulism neurotoxin
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Foodborne botulism
Symptoms
A rapidly progressive descending symmetrical paralysis
Foodborne/ wound botulism
• Possible D and V
• Diplopia
• dysphagia or dysarthria
• dry mouth
• Hypotension
• Urinary retention, or
constipation.
• Respiratory failure, Cardiac
arrest
• Diminished or absent deep
tendon reflexes
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Foodborne botulism
Infant Botulism
Less specific:
• Constipation, irritability followed
by Lethargy
• Poor feeding
• Poor sucking
• Drooling
• Hypotonia
• General weakness
not usually present: elevated blood
pressure ; fever; altered mental state;
altered sensation;
Differential diagnosis:
Myasthenia gravis: Tensilon test positive
Guillain-Barre syndrome:
Ascending paralysis, CSF protein elevated
Miller-Fisher Syndrome
Descending paralysis
Presence of anti-ganglioside antibodies:
CSF protein elevated.
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Foodborne botulism
Laboratory confirmation of botulism
Botulism is a Clinical Diagnosis
Detection of toxin
Detection of the organism by:
Culture and isolation
Detection of toxin
of C. botulinum
genes A,B,E, F
Food, faeces, rectal wash,
Food, serum, faeces, rectal
pus, tissue
wash
Real time PCR
M.B.A.
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Foodborne botulism
Food, faeces, rectal wash
out, wound tissue, pus,
environmental samples
Specimens to send to the
reference laboratory (Colindale)
Foodborne botulism:
Toxin detection by MBA:
• Serum (2-10ml) NOT haemolysed – NOT plasma
• Stool and others (vomitus, gastric contents, intestinal contents)
• Food frozen except for tins and jars
Detection of the organism by toxin gene detection (PCR) and
culture:
• Stool in anaerobic broth (ex: CMB – Robinson – FAB)
• Food
• Others – vomitus, gastric contents…in anaerobic broth
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Foodborne botulism
Specimens to send to the
reference laboratory (Colindale)
Infant botulism
Detection of the organism by toxin gene detection (PCR) and culture:
• Stool or rectal wash out in anaerobic broth
• Food (honey)
• Dust and environment samples (water sediment – pet food)
Toxin detection:
• Stool
• Rarely: serum
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Foodborne botulism
Specimens to send to the
reference laboratory (colindale)
Wound botulism
Toxin detection:
• Serum (2-10ml)
Detection of the organism by toxin gene detection (PCR) and culture:
• Pus, debrided tissue in anaerobic broth
• Heroin
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Foodborne botulism
Timing of specimens is important
Serum: within 2 days of onset of symptoms
Neurotoxin detected in serum and faeces
>50% within 1 day of onset
<25% of cases after 3 days
Faeces: within a week of onset:
C. botulinum detected in faeces
>70% within 2 days
40% after 10 days
Immunity to botulism does not develop, even with severe
disease – repeated occurrence of botulism has been reported.
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Foodborne botulism
Foodborne botulism in the UK and Ireland 1922-1989
20
Year
Cases
Deaths
Food
Toxin type
1922
8
8
Duck pate
A
1932
2
1
Home made rabbit and pigeon broth
NK
1934
1
0
Home made jugged hare
NK
1935
?5
?4
Home made nut brawn
A
1935
1
1
Home made minced meat pie
B
1949
5
1
Home made macaroni cheese
NK
1955
2
0
Pickled fish
A
1978
4
2
Canned salmon
E
1987
1
0
Airline meal (rice and veg)
A
1989
27
1
Hazelnut yoghurt
B
Foodborne botulism
Foodborne botulism in the UK and Ireland, 1998-2011
21
Year
Cases
Food
Preparation and origin
Toxin type
1998
2
Bottled mushrooms
Home made in Italy
B
2003
1
Sausage
Home made in Poland
B
2004
1
Hummus
Commercial, UK
Not
confirmed
2005
1
Not known
returned from Georgia
A
2005
1
Preserved pork
Home made in Poland
B
2006
1
Preserved pork
Home made in Poland
A/B
2008
1
Polish sausages
Polish national in Ireland
B
2010
1
Not known
Returned from Algeria
B
2011
3
Korma sauce
Commercially prepared, UK
A
2012
1
Olives
From Italy, distributed in Europe
B
Foodborne botulism
Foodborne botulism July 2012 - Olives
14th July: A 46 year old female Oxfordshire resident has a
lunch/dinner party at friends.
15th July: she developed mild symptoms of blurred vision, dry
mouth.
18th July: she goes to her GP who takes a blood specimen.
19th July: Admitted to hospital, seen by neurologist on the 20th
when the patient developed poor swallowing – the neurologist
suggests botulism as diagnosis.
The patient is monitored – not ventilated
Cranial bilateral bulbar palsy
Proximal upper limb weakness
No sensory loss
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Foodborne botulism
Foodborne botulism July 2012 - Olives
1 week after onset of symptoms…
22nd July: Hospital contacts duty doctor in Colindale for obtaining
antitoxins.
23rd July: Reference laboratory contacted by duty doctor.
Follow a series of phone calls between Reference laboratory and
the hospital – consultant micro, the ITU and Thames Valley HPU.
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Foodborne botulism
Foodborne botulism July 2012 - Olives
The patient ate at the party. She was the only one with
symptoms and the only one to have eaten olives at the party.
Another guest spat out an olive saying it did not taste right.
The olives were then put aside to be disposed of, but stay on a
table at room temperature while the hosts went for a week
abroad on holiday.
When the host came back, they learned their friend was ill,
called the hospital and suggested the olives was the cause of
illness.
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Foodborne botulism
Foodborne botulism July 2012 - Olives
23rd July, at 17:20
The olives arrived at Colindale.
•
•
•
•
•
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The original jar with olives – pH 6.65
A sterile container with olives (the original was leaking)
A CMB with a rectal swab DOC 22.07.12 – 7 days after onset of symptoms
Serum DOC 18.07.12 taken by GP – 3 days after onset of symptoms
Serum DOC 22.07.12 – pre-IG treatment – 7 days after onset of symptoms
Foodborne botulism
Foodborne botulism July 2012 - Olives
24th July,
The olives:
10:30 - PCR results – POSITIVE for neurotoxin gene B
11:30 – MBA results – POSITIVE for typical symptoms of botulism
(neutralisation tests were performed the next day and detected neurotoxin B)
The clinical specimens:
• Rectal swab - negative
• Serum – negative
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Foodborne botulism
FSA alerted
National recall of olives and warming
not to eat from this batch
Foodborne botulism July 2012 - Olives
25th July, 10 days after onset of symptoms, a faecal specimen is collected
from the patient, now at home.
27th July, Friday:
A stool specimen arrived at Colindale. It can not be tested on receipt because
it is not in a broth.
Broth inoculated with the stool specimen – incubated overnight
30th July Monday:
PCR results – POSITIVE for neurotoxin gene B
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Foodborne botulism
Foodborne botulism Scotland 2011
8th November:
A 5 year old child developed diplopia and dysphagia – taken to GP who sent
the child back home.
During the night, child became very unwell, unable to swallow, drooling,
taken to GP again then to hospital in Sterling.
Child had to be ventilated and was taken to Children’s Hospital PICU in
Glasgow.
On same day in the afternoon, the 7 year old sister developed blurred vision.
9th November: the 7 year old sister developed sore throat – admitted to
Sterling Hospital and when deteriorating was taken to PICU in Glasgow and
ventilated.
NO D&V - no fever – CT scan and MRI normal – LP normal
Neurology and immunology team: botulism as the most likely diagnosis
Children received antitoxin and stabilised
Colindale alerted
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Foodborne botulism
Foodborne botulism – Scotland 2011
10th November: first teleconference
• Children received antitoxin and stabilised
• The parents and the 3 year old sibling have no symptoms.
• Food history: try to identify plausible foods eaten within 36h
from onset of symptoms, by the children only.
Olives in jar (lots of discussion about olives because of recent
botulism outbreak in Helsinki and France)
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Foodborne botulism
Foodborne botulism – Scotland 2011
Olives in jar
Carrots
Pitta bread
Humus
Curry sauce in jar with chicken: dad said ‘ smell funny’ but gave it to
the children
Hot dogs
Cheese
Chicken nuggets
Sun dried tomatoes in oil
Rice
Potatoes
Peppers
Vanilla yoghurt
Salad
Smoothies
biscuits
Cereal
Banana milkshake
Frozen raspberries
honey
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Foodborne botulism
Foodborne botulism – Scotland 2011
IN
Olives in jar
Curry Sauce in jar
Yoghurt
Honey
Pitta Bread
Humus
Sundried tomatoes
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Foodborne botulism
OUT
Grilled chicken
Homemade biscuits
Carrots
Raspberries
Pasta, chicken, tomato sauce
broccoli
Cereal
Banana Milkshake
Foodborne botulism – Scotland 2011
Food item
Specimen information
M&S wholemeal Pittas
From rubbish bin
Remnant of Korma
sauce +Chicken
From wheelie bin
Toxin detection
C. botulinum Comments on PCR
by MBA
detection by PCR results
Spores only
Not detected
C. botulinum A
detected.
Toxin A detected
C. botulinum A
Vegetative cells and
spores detected
Lid from the consumed
From rubbish wheelie bin Toxin A detected
korma sauce jar
C. botulinum A
Vegetative cells and
spores detected
Empty jar of consumed
korma sauce
Vegetative cells and
spores detected
From recycling bin
Toxin A detected
C. botulinum A
Opened but not
consumed; From dry good
cupboard
Not detected
Negative
Empty container of
olives
From wheelie bin
Not detected
Negative
Oil from sun-dried
tomatoes
From fridge
Not detected
Negative
Houmous
From fridge
Not detected
Negative
Korma sauce jar
FSA issued National product recall
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Foodborne botulism
Patient
specimen
information
Date of
collection
Toxin detection by MBA
C. botulinum
detection by PCR
Boy
Serum
08.11.11
Not performed/ haemolysed
NA
boy
Blood
09.11.11
Not performed/ haemolysed
NA
Boy
Blood
09.11.11
Not performed/ EDTA treated
NA
Girl
Serum
09.11.11
NA
Boy
Serum
09.11.11
Toxin detected - Classic symptoms
of botulism observed, insufficient
serum for confirmatory
neutralisation test
Girl
Blood
10.11.11
Not performed/ haemolysed
NA
Girl
Blood
10.11.11
Not performed/ EDTA treated
NA
10.11.11
Not performed
C. botulinum A
10.11.11
Not performed
C. botulinum A
Girl
Boy
33
Rectal washout in
Anaerobic broth
Rectal washout in
Anaerobic broth
NA
Boy
Rectal washout
10.11.11
Not detected
C. botulinum A
Boy
Gastric aspirate
10.11.11
Not detected
Negative
Girl
Gastric aspirate
10.11.11
Not detected
Negative
Girl
Rectal washout
10.11.11
Not detected
Negative
Foodborne botulism
Foodborne botulism – Scotland 2011
16th November:
3rd sibling, a 3 year old girl, admitted to hospital after choking on
food – gagged on food collapsed a few time and eyes were
droopy.
Taken to A&E with ptosis – then discharged the next day !
17th November:
Choked on food again – antitoxin given
23rd November:
Stool specimen for 3 year old PCR Positive for neurotoxin gene A
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Foodborne botulism
How to prevent foodborne botulism
C. botulinum has to grow to produce toxin.
The main limiting factors for growth of C. botulinum in foods are:
1. temperature, (optimum growth is 35°C or 25°C)
2. pH, below 4.6
3. water activity, (min aw of ~0.94 is needed for growth) 10% NaCl
4. redox potential, presence of oxygen
5. food preservatives, (nitrite, sorbic acid, polyphosphates..)
6. competing microorganisms, lactic acid bacteria, intestinal
microflora.
7. ‘Botulinum cook’: pressure cooker 121°C for 3 minutes
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Foodborne botulism
Who to speak to???
Clinical diagnosis:
• Consult neurologist and local ID Physician
• Botulism duty doctor protocol (HPA website)
Microbiology confirmation and Guidelines and advice on
specimens, availability and interpretation of results:
• Reference laboratory Colindale
• GBRU User Manual (LGP user manual HPA website)
• Dr Corinne Amar or Dr Kathie Grant
Availability of antitoxin:
• Duty doctor in Colindale
• BabyBIG: Infant Botulism Treatment and Prevention
Programme, California, USA. http://www.infantbotulism.org/
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Foodborne botulism
Thank You,
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Foodborne botulism