Annex B: Micro-organisms · There are two types of food poisoning caused by B. cereus: (1) nausea and vomiting similar to symptoms of St. aureus poisoning caused by an emetic toxin

Annex B: Micro-organisms

B.1 Pathogens

Table B1 summarises the sources and symptoms of pathogenic bacteria and the fol-

lowing section is a brief description of each pathogen.

B.1.1 Aeromonas spp.

Three species of Aeromonas are thought to be responsible for gastroenteritis, partic-

ularly in immunocompromised people or people suffering from cancer: A. hydrophi-

lia HG 1, A, A. caviae HG 4 and A, and A. veronii HG 8, although their role as an

enteropathogen has not been definitively established. In healthy people, children

below 5 years old are at greatest risk. Two types of symptoms are mild diarrhoea

and a severe illness similar to cholera that may be life-threatening. A. hydrophilia is

also associated with a range of other illnesses, including inflammation of the gall-

bladder, septicaemia and meningitis, which can cause death in more than 60% of

cases (Motarjemi, 2002; Sutherland and Varnam, 2002). The pathogen invades cells

in the intestine and although it is known to produce toxins, their role has not been

definitely established. It has been found in water and a wide range of foods, includ-

ing vegetables, meat and poultry and fish and shrimps, although it is possible that

its presence in these foods is due to contaminated water used in processing.

B.1.2 Bacillus cereus

There are two types of food poisoning caused by B. cereus: (1) nausea and vomiting

similar to symptoms of St. aureus poisoning caused by an emetic toxin produced in

foods; and (2) diarrhoea and abdominal pain without vomiting, similar to symptoms

of Cl. perfringens toxin, caused by diarrhoeagenic toxins produced in the small

intestine. The minimum cell concentration for both types of illness is approximately

105 cells. Because both types of symptoms are relatively mild and short-lived, the

incidence of B. cereus food poisoning is thought to be significantly underreported.

The emetic type is mostly associated with rice products, where spores survive heat-

ing and germinate in the cooling product, producing toxins in the food. The diar-

rhoeal type of toxin is found in meat, milk and vegetable products where cells

survive heat processing, multiply sufficiently before consumption and produce tox-

ins in the intestine. Other species, similar to B. cereus, also cause food poisoning

including B. subtilis, B. licheniformis and B. thuringiensis. B. subtilis causes acute

vomiting within 2�3 hours of consumption, followed by diarrhoea, whereas

Table

B1Sources

andsymptomsofpathogenic

bacteria

Pathogen

Sources

Minim

um

growth

conditions

D-value

z-value

(�C)

Symptomsofinfection

Typicalhigh-

risk

foods

Tem

perature

(�C)

pH

aw

Aerobacter

spp.

Warm

bloodied

anim

als

15

5.5

Abdominal

pain,

diarrhoea

within

24�7

2h

Aeromonas

hydrophilia

Fresh

or

brackish

water

1�5

Diarrhoea,vomiting,

fever

within

12�3

6h

Water,vegetables,

cheese,rawmilk,

poultry,lambor

shellfish

Bacilluscereus

Soil,surfaces

of

cereals,

vegetables

andmeats

4(psychrotrophic

strains)

35

(mesophilic

strains)

4.3

0.91�0

.95

1.2�8

min

at

100� C

6�9

Twotypes:em

etic

nauseawithin

1�5

h

ordiarrhoea

within

8�1

6h

Reheatedrice

and

products

containingcereals

orspices

(emetic

type),meat

products,sauces,

milkproducts

(diarrhoealtype)

Brucellaspp.

Farm

anim

als

Acute

jointand

muscle

pain,fatigue.

Chronic

genitourinary,

cardiovascularand

neurological

conditions

Raw

milk,

unpasteurised

dairy

products

Campylobacter

jejuni

Warm

bloodied

anim

als

.25

3.6

1min

at55� C

5Diarrhoea,headache,

abdominal

pain,

within

24�7

2h

Poultry

products,

raw

milkandto

lesser

extent

meatandmilk

products,water,

shellfish

Clostridium

botulinum

Ubiquitous,

especially

soiland

water

10

4.7

0.94

25min

at

100� C

and

0.1�0

.2min

at121� C

Seven

types

oftoxin:

vomiting,blurred

vision,progressive

difficultyin

swallowing,respiratory

failurewithin12�3

6h.

Upto70%

fatal

Canned

vegetables

andother

low-

acid

foods,

smoked

fish

GroupI

3.3

5.0

0.97

GroupII

,0.1min

at

100� C

and

,0.001min

at121� C

Clostridium

perfringens

Ubiquitous�

soil,raw,

dried

and

cooked

foods

12

5.5

0.95

1�3

min

at

95� C

(heat-

sensitive

spores)

Acute

diarrhoea,

flatulence

within

8�1

8h,butlittle

nauseafever

or

vomiting

Cooked

andraw

meats,poultry,

fish,dairy

products,dried

foods(e.g.soups,

spices,pasta)

18�6

4mins

(heat-

resistant

spores)

Enteropathogenic

Escherichia

coli

Intestinal

tract

ofhumans

andwarm-

blooded

anim

als

7�8

4.4

0.95

Sixtypes

ofillness

includingintestinal

haemorrhage,bladder/

kidney

infections,

septicaem

ia,blood

clotsonbrainwithin

7h�4

days.aSome

types

fatal

Meat,poultry,fish

vegetables,soft

cheeses,water,

alfalfashoots

(alltypes)

6.5

(O157:H7)

Listeria

monocytogenes

Ubiquitous�

soil,most

foods,

healthy

humansor

anim

als,

surfaces

20.4

4.39

0.92

Adults:gastroenteritis

within

24�4

8h.

New

born

babies:

meningitisanddeath.

Unborn

foetus:

spontaneousabortion,

stillbirth

ormeningitis.

Individualshaving

compromised

immune

Milk,seafoods,

smoked

or

marinated

fish,

sandwiches,raw

vegetables/salads,

coleslaw

,raw

or

cooked

meats/

pate,poultry

products,soft

cheeses (Continued)

Table

B1(C

ontinued)

Pathogen

Sources

Minim

um

growth

conditions

D-value

z-value

(�C)

Symptomsofinfection

Typicalhigh-

risk

foods

Tem

perature

(�C)

pH

aw

system

s:meningitisor

septicaem

ia

Mycobacterium

avium

subspp.

paratuberculosis

Milk

25

5.5

12s(at71� C

in

milk)

8.6

Associated

withCrohn’s

disease

Milkandmilk

products

Plesiomonas

shigelloides

Fresh

water

Diarrhoea,abdominal

pain,nauseawithin

24�4

8h

Water

orshellfish

Salmonella

enterica

Poultry,cattle,

pigs,other

anim

als

5.2b

3.8c

0.94

0.28�1

0s(in

milk)

Gastroenteritis(w

ithin

12�4

8h,duration

2�7

days):nausea,

vomiting,highfever,

abdominal

pain,may

befatal

Eggs,poultry,milk,

cooked

meats,

salami,cheeses

0.36min

(in

groundbeef)

0.55�9

.5min

(inliquid

egg),

4.5�6

.6h

(in

chocolate)

Entericfever

(within

7�2

8days,duration

14days):highfever,

nausea,abdominal

pain.Carrier

for

months/years

Septicaem

ia:highfever,

abdominal

and

thoracicpain

Shigella

spp.

Infected

people,

foodorwater

Dysentery,severe

abdominal

pain,fever

within

12�5

0h

Salads,milk,soft

cheese,cooked

rice

Staphylococcus

aureus

Anim

als,

human

skin

andnasal

cavity,

surfaces

7(10fortoxin

production)

Nausea,vomiting,

sometim

esdiarrhoea,

within

2�4

h

Recontaminated

heat-processed

foods,cheese,

salami,cooked

meats,dried

milk,sandwiches

Vibrio

parahaem

olyticus,

V.cholerae

Inshore

marine

waters

5�1

0Gastroenteritis,

abdominal

cram

ps,

nausea,fever,within

4�2

4h.Cholera

(V.

cholerae)

within

6h�3

days

Raw

,im

properly

cooked

or

recontaminated

fish

andshellfish,

water

Yersinia

enterocolitica

Pigs

21�7

Fever,diarrhoea,severe

abdominal

pain,

vomiting,jointpain

within

24�3

6h

Pork,milk,tofu,

chitterlings(pork

intestine)

aSee

textfordetails.

bMostserotypes

donotgrow,7� C

.cMostserotypes

donotgrowbelow

pH

4.5.

Source:

Dataadaptedfrom

Bell,C.,Kyriakides,A.,2002a.Pathogenic

Escherichia

coli.In:deW.Blackburn,C.,McC

lure,P.J.(Eds.),FoodbornePathogens�

Hazards,RiskAnalysisandControl.WoodheadPublishing,Cam

bridge,

pp.279�3

06;Bell,C.,Kyriakides,A.,2002b.Salmonella.In:deW.Blackburn,C.,McC



bridge,pp.307�3

35;Park,R.W

.A.,

Griffiths,P.L.,Moreno,G.S.,1991.Sources

andsurvival

ofcampylobacters

�relevance

toenteritisandthefoodindustry.J.Appl.Bacteriol.70,S97�S

106;McC

lure,P.,deW.Blackburn,C.,2002.Cam

pylobacterandArcobacter.

In:deW.Blackburn,C.,McClure,P.J.(Eds.),FoodbornePathogens�


bridge,pp.363�3

84;Sutherland,J.,Varnam

,A.,2002.Enterotoxin-producingStaphylococcus,

Shigella,Yersinia,Vibrio,Aeromonas

andPlesimona.In:deW.Blackburn,C.,McClure,P.J.(Eds.),FoodbornePathogens�


bridge,pp.386�4

15;Gibbs,P.,2002.

Characteristicsofspore-form

ingbacteria.In:deW.Blackburn,C.,McClure,P.J.(Eds.),FoodbornePathogens�


bridge,pp.418�4

35;Griffiths,M.,2002.

Mycobacterium

paratuberculosis.In:deW.Blackburn,C.,McC



bridge,pp.489�5

00.

B. licheniformis causes diarrhoea within 8 hours, sometimes with vomiting. They

grow in foods mainly as a result of temperature abuse and numbers exceeding 106

can cause intoxication. B. thuringiensis is also known to produce toxins and con-

cern has been expressed over its use as an insecticide on vegetables (it is lethal to

cabbage white caterpillars) (Gibbs, 2002).

B.1.3 Brucella spp.

The strains of Brucella spp. that cause human brucellosis are B. abortis (from

cows), B. melitensis (from sheep and goats) and B. suis (from pigs). People working

closely with farm animals mainly contract the disease but it can also be contracted

by consumption of raw milk and unpasteurised dairy products. The acute symptoms

include fatigue, weakness, muscle and joint pain and weight loss within 2 months

of infection. It can also result in chronic health problems including inflammation of

joints, genitourinary, cardiovascular and neurological conditions and insomnia and

depression (Motarjemi, 2002).

B.1.4 Campylobacter spp. and Arcobacter spp.

Campylobacter jejuni is the most important pathogen in this group, causing up to

90% of reported campylobacteriosis infections, with C. coli also causing less com-

mon illnesses. Before 1991, two species of Arcobacter (A. butzleri and A. cryaero-

philus) were known as aerotolerant Campylobacter. They have been associated with

enteritis in humans and abortions and enteritis in animals, but have not been linked

to widespread outbreaks of food poisoning. Both Campylobacter and Arcobacter

are normal intestinal flora of animals and poultry, and illness is usually caused by

eating recontaminated foods or foods that are raw or inadequately cooked.

Campylobacter jejuni is an important cause of sporadic gastroenteritis because,

even though the cells do not survive for long periods in foods, they are highly viru-

lent and only a few hundred cells are needed to cause infection. C. jejuni is thermo-

philic (optimum 37�42�C), but can survive at low temperatures. It is sensitive to

heating, drying, freezing, acidity, oxygen and low concentrations (2%) of salt. The

higher incidence of illness in very young children may indicate that there is protec-

tive immunity after infection. Immunocompromised people have a severe and pro-

longed illness, septicaemia or other infections. C. jejuni infection is also associated

with development of Guillain�Barre syndrome (GBS), an autoimmune disease that

causes limb weakness and paralysis that is sometimes fatal. It can also cause

chronic arthritis, meningitis, abortion and neonatal sepsis (Motarjemi, 2002). C.

jejuni can form viable but nonculturable (VBNC) cells that are metabolically active

but cannot be made to grow by culturing. This can be brought about by sublethal

environmental conditions such as freeze�thaw injury. However, outbreaks of ill-

ness from VBNC cells are possible, indicating that they may recover in the intes-

tines (McClure and Blackburn, 2002).

e38 Annex B: Micro-organisms

B.1.4.1 Clostridium botulinum

Although bacteria of the genus Clostridia can be anaerobic to aerotolerant,

Clostridium botulinum is strictly anaerobic and can only sporulate under anaerobic

conditions. It is widely distributed in soils and marine and freshwater sediments.

There are four phenotypes (numbered I�IV) but only groups I and II produce sig-

nificant food poisoning. The different toxins produced by Cl. botulinum are labelled

A�G, with Group I proteolytic bacteria producing A, B and F toxins and Group II

nonproteolytic bacteria producing B, E and F toxins. The toxins are among the

most poisonous of natural toxins and block acetylcholine release across nerve syn-

apses to cause muscular paralysis. Symptoms of botulism usually appear within

12�36 hours, but may be delayed by up to 10 days. They include vomiting and

nausea, quickly followed by double vision, speech impediment and difficulty in

swallowing. This is followed by general muscular weakness, lack of coordination

and respiratory failure. An antitoxin has been developed which reduces the mortal-

ity rate when it is administered quickly, but patients may still require artificial res-

piration to enable recovery. Because of the severity of the intoxication, particular

care is taken by the canning industry to ensure that correct time/temperature combi-

nations are used, and the incidence of poisoning from commercial products is low.

Most cases arise from home vegetable canning (in the United States), improperly

cured or undercooked fish or meats, or inclusion of fresh herbs and spices in cook-

ing oils (Gibbs, 2002).

B.1.4.2 Clostridium perfringens

Different strains (A�E) of Cl. perfringens (previously Cl. welchii) produce some of

the four main types of enterotoxin. Type A Cl. perfringens is most common and

results in relatively mild poisoning that lasts for about 24 hours. Because of the

short duration and relatively mild symptoms this type of poisoning is thought to be

severely underreported (Gibbs, 2002). Cl. perfringens has a relatively high optimum

temperature for growth (43�45�C) and can grow up to 50�C, doubling in number

every 8�10 minutes under optimum conditions, making it one of the fastest-

growing food-poisoning bacteria. The main sources are cooked meats that suffer

temperature abuse or inadequate refrigeration after cooking. Inadequate cooking

can also stimulate spore germination on cooling. Refrigeration or freezing kills cells

but spores may survive to germinate and grow rapidly on reheating or thawing. Cell

growth is inhibited by 6�8% salt and up to 400 μg/kg of nitrite, and properly cured

meats are not usually a source of this pathogen.

B.1.5 Enteropathogenic Escherichia coli

E. coli is the most common nonpathogenic flora in the human intestine and it has

long been used as an indicator of faecal contamination of foods. Some strains have

developed the ability to cause disease and illnesses attributed to E. coli have been

acknowledged for 100 years. However, in recent years attention has increased

e39Annex B: Micro-organisms

because of significant morbidity and mortality in food-poisoning outbreaks, particu-

larly those associated with vero cytotoxin-producing E. coli (or VTEC). In indus-

trialised countries the focus has been on E. coli O157:H7, but others including E.

coli O26, O103, O111, O118 and O145 may pose an equal or greater threat to pub-

lic health (Bell and Kyriakides, 2002a). Of the pathogenic types of VTEC, there are

differences in the virulence genes that result in six types of pathogenicity identified

so far (Bell and Kyriakides, 2002a; Scaletsky et al., 2002):

1. Enteropathogenic E. coli (EPEC) � onset within 9�72 hours, duration 6 hours�3 days.

These types invade mucosal cells causing severe diarrhoea, fever, vomiting and abdominal

cramps.

2. Enterotoxigenic E. coli (ETEC) � onset within 8�44 hours, duration 3�19 days. These

adhere to small intestine mucosa and produce toxins that act on mucosal cells causing

diarrhoea, cramps and nausea.

3. Enteroinvasive E. coli (EIEC) � onset within 8�72 hours, duration days�weeks. These

types invade epithelial cells in the colon causing dysentery, vomiting, fever, headache and

abdominal cramps.

4. Enterohaemorrhagic E. coli (EHEC) � onset within 3�9 days, duration 2�9 days. These

serotypes, including E. coli O157:H7, attach to mucosal cells and produce potent toxins,

causing severe abdominal pain, bloody diarrhoea and vomiting but no fever. In young

children and the elderly they may cause acute renal failure, seizures, coma and death.

5. Enteroaggregative E. coli (EAEC) � onset within 7�48 hours, duration 14 days�weeks.

These types bind in clumps to cells of the small intestine and produce toxins that cause

persistent diarrhoea but not fever or vomiting.

6. Diffusely adherent E. coli (DAEC) � onset and duration not yet established.

Epidemiology and clinical profiles of the illness are not yet established, but may cause

diarrhoea in older children.

Methods to identify and control VTEC are described by Bell and Kyriakides

(2002a).

B.1.5.1 Listeria monocytogenes

This is the most important pathogen among six Listeria species and it has two sero-

types (4b and 1/2a). Listeriosis is rare and in healthy adults only causes mild flu-

like symptoms or vomiting and diarrhoea when large numbers of cells are ingested.

However, if elderly people or people who have compromised immune systems (e.g.

patients taking immunosuppressant drugs after organ transplants, HIV/AIDS infec-

tion or cancer treatment), become infected they can develop meningitis, encephalitis

and/or septicaemia, often with high mortality rates (Motarjemi, 2002). Cross-

infection in maternity hospitals and foodborne infections are the main sources of

transmission. If pregnant women become infected Listeria can cause infection of

the uterus, bloodstream or central nervous system, resulting in spontaneous abor-

tion, stillbirth, or infection of the foetus and birth of a premature severely ill baby.

L. monocytogenes is psychrotrophic and can grow at refrigeration temperatures, and

national and international standards as well as food company specifications describe

maximum levels of contamination, especially for chilled and ready-to-eat foods.


Methods to identify and control L. monocytogenes are described by Bell and

Kyriakides (2002b).

B.1.5.2 Mycobacterium paratuberculosis

Now known as Mycobacterium avium subspp. paratuberculosis, this bacterium

causes Johne’s disease in cattle and has been associated with the similar Crohn’s

disease in humans (incurable highly debilitating chronic inflammation of the gastro-

intestinal tract). It has been found in pasteurised milk but the results of a number of

studies of its ability to survive pasteurisation conditions remain inconclusive

(Griffiths, 2002).

B.1.6 Plesiomonas spp.

A single species, Pl. shigelloides, shares similar characteristics to both Vibrio spp.

and Aeromonas spp. It causes three types of diarrhoeal symptoms: secretory and

shigella-like, both of which are more common and can vary in severity, and the less

common cholera-like symptoms. It can also cause meningitis and has a mortality

rate of � 80% (Sutherland and Varnam, 2002). It can invade intestinal cells and

also has the ability to produce enterotoxins, protease, elastase and haemolysin.

People at most risk include young children, the elderly and those suffering from

cancer. Plesiomonas is found in fresh water and illness is most often caused by

drinking contaminated water or eating raw shellfish from such water.

B.1.7 Salmonella spp.

Salmonella spp. are among the most important causes of foodborne disease world-

wide and an individual outbreak may affect several thousand people at a time.

Symptoms range from mild/severe food poisoning (gastroenteritis) to severe

typhoid, paratyphoid and septicaemia. These severe conditions produce high rates

of morbidity and mortality. There are an estimated 2400 serotypes, mostly desig-

nated as the species S. enterica, but new strains are evolving, some of which exhibit

multiple antibiotic resistance. Salmonella spp. cause illness by invading intestinal

cells and releasing an enterotoxin that causes inflammation and diarrhoea. They can

also enter blood vessels and the lymphatic system to cause the more severe ill-

nesses, including reactive arthritis, pancreatitis, osteomyelitis and meningitis. The

numbers of ingested cells needed to cause illness is .10,000, but may be as low as

10�100 cells when infected fatty foods such as cheese or salami are eaten and the

fat protects the cells. Salmonella may persist in faeces after recovery from illness,

making the person a carrier and thus a potential hazard if employed as a food han-

dler. The above data and methods to identify and control Salmonella are described

by Bell and Kyriakides (2002c). Because of its importance, specified levels of

Salmonella spp. in foods (negative in 25 g samples) are incorporated into national

legislation and international standards. Some serotypes are able to survive for long

periods under frozen storage (e.g. 4 months in poultry and minced beef at �18�C,


or 7 years in ice cream at �23�C) and under conditions of low aw (e.g. 9 months in

chocolate at aw5 0.41 and 6 weeks in peanut butter at aw5 0.2�0.33) (Bell and

Kyriakides, 2002c).

B.1.8 Shigella spp.

The genus Shigella of the Enterobacteriaceae family has four subgroups (Sh. dysen-

teriae, Sh. flexneri, Sh. boydii and Sh. sonnei). They infect people mainly by

person-to-person transmission and contaminated food and water in areas that have

poor hygienic standards. The bacteria multiply in the colon and invade epithelial

cells where they cause ulcerative lesions. Sh. dysenteriae produces a heat-sensitive

cytotoxin (shiga toxin) which kills the colon cells, and it may also produce an

enterotoxin and neurotoxin. Among healthy adults it causes symptoms that may last

for 3�4 days, but is rarely a cause of death. However, it may cause convulsions

and delirium and is a common cause of mortality among immunocompromised peo-

ple and among infants in places where hygiene is poor. Shigella is not found in the

general environment and most infections are caused either by people who are car-

riers and infect foods, or by faecal contamination of crops. In practice almost any

food could be a source of contamination if hygiene standards are low and there is a

high incidence of Shigella infection in the general population.

B.1.9 Staphylococcus aureus

This pathogen is a normal part of the flora that is found on the skin and in nasal

cavities of humans and animals. It can produce up to 11 enterotoxins when growing

in food and intoxication can result from eating as little as 94�184 ng of one of the

toxins (Varnam and Evans, 1996). However, substantial cell growth is needed to

produce sufficient toxin to cause illness and toxin production is more easily inhib-

ited than cell growth by control of aw and pH. The toxins differ from other entero-

toxins in that they do not act directly on cells in the intestine, but act more like a

neurotoxin, stimulating nerves that in turn stimulate the vomiting centre in the brain

(Sutherland and Varnam, 2002). Symptoms rarely last more than 24 hours followed

by rapid recovery, and deaths are rare. This relatively mild intoxication may be

responsible for significant underreporting of St. aureus illnesses. St. aureus cells are

readily destroyed by normal heating conditions used in processing, but the toxin is

not. It is therefore possible for foods such as pasteurised dried milk and salami to

contain the toxin without evidence of cellular contamination. Cells are unable to

grow below 7�C and toxins are not produced below 10�C, thus making refrigeration

the best method of control for products that are not heated. St. aureus is more resis-

tant to preservatives such as salt and sodium nitrite than many pathogens, enabling

it to grow in cured meats. It is also able to grow in vacuum-packed and MAP foods

(see Section 24.3), although toxin production may be inhibited. Its relatively high

tolerance to low aw compared to other bacteria allows it to grow during manufac-

ture of dried and intermediate moisture products.


B.1.10 Vibrio spp.

There are 10 Vibrio species that cause gastrointestinal illness, the most important

being V. parahaemolyticus and V. cholerae, the latter causing Asiatic cholera.

Another (V. vulnificus) also causes septicaemia. They are associated with seawater

and seafood is the most common source of foodborne infection, although V. choler-

ae is also associated with contaminated fresh water as well as foods. V. cholerae

has two serotypes (O1 and O139) that produce a number of enterotoxins, including

haemolysins and cytotoxins. They cause copious diarrhoea within 6 hours to 3

days, with rapid loss of body fluids and mineral salts causing dehydration and lead-

ing to death if not treated by rehydration and salt replacement. Nontoxigenic strains

cause less severe gastroenteritis, abdominal cramps and fever. In contrast, V. para-

haemolyticus is an invasive nontoxigenic pathogen, which causes diarrhoea that

lasts for 2�3 days, rarely causing death. There is also a more severe strain that pro-

duces Shiga-like cytotoxin and enterotoxin and causes dysentery. It is associated

with consumption of raw fish and seafoods, or cooked seafoods that are recontami-

nated due to poor hygiene. In healthy people, V. vulnificus causes mild gastroenteri-

tis but in people suffering from medical conditions, including hepatitis, cirrhosis or

gastric disease, it causes skin lesions and septicaemia, resulting in death in approxi-

mately 50% of cases. It destroys body tissues by secreting haemolysins, proteinases,

collagenases and phospholipases. It is strongly associated with consumption of raw

oysters, particularly in summer months when seawater temperatures are higher

(Sutherland and Varnam, 2002).

B.1.11 Yersinia enterocolitica

Yersinia enterocolitica, and to a lesser extent Y. pseudotuberculosis, are infectious

foodborne pathogens associated mostly with pork. They are members of the family

Enterobacteriaceae but unlike most other bacteria in this family, Y. enterocolitica

is able to grow at 4�C. In addition to the symptoms in healthy adults caused by

infection of the intestinal tract, it may cause autoimmune thyroid disease, liver

abscesses, pneumonia, septicaemia tissue infections, conjunctivitis and pharyngitis,

especially among elderly and immunocompromised people. Children aged from

young infants to young teenagers are most susceptible to infection. Y. enterocolitica

is not especially heat-resistant and is destroyed at normal processing temperatures.

However, recontamination of processed food is important because of its ability to

grow at refrigeration temperatures. It is not inhibited by vacuum packing but is

sensitive to carbon dioxide used in MAP (see Section 24.3) (Sutherland and

Varnam, 2002).

B.2 Viruses

Table B2 describes the characteristics of viral foodborne infections.


Table

B2Characteristics

ofviralfoodborneinfections

Virustype

Incubation

time

Symptoms

Agegroupsatrisk

Durationof

illness

Severity

Adenovirus

7�1

4days

Diarrhoea

Children,5years

Days/weeks

Mild

Astrovirus

24�4

8h

Diarrhoea

Children,10years

Days

Mild

Calicivirus

24�4

8h

Vomiting/diarrhoea

All(especially

institutionalised

or

hospitalised

people)

Days

Mild

Enterovirus

1�2

weeks

Diarrhoea,meningitis,

encephalitis,paralyticillness

Children,15years

Days/weeks,can

belife-long

Can

besevere

HepatitisA

Upto

50

days

Hepatitis

Allifendem

icWeeks

Severityincreaseswithage

offirstinfection

HepatitisE

Upto

70

days

Hepatitis

All

Weeks

Mildexceptforpregnant

women

Rotavirus

24�4

8h

Vomiting,diarrhoea,fever

Children,5years

Days

Majorcause

ofdeath

in

developingcountries

Source:

Adaptedfrom

Koopmans,M.,2002.Viruses.In:deW.Blackburn,C.,McC


Hazards,RiskAnalysisandControl.Woodhead

Publishing,Cam

bridge,pp.440�4

52.

Table

B3Enzymes

from

GM

microorganismsusedin

foodprocessing

Enzyme

Host

organism

Donororganism

Application

α-A

cetolactate

decarboxylase

Bacillusamyloliquefaciensorsubtilis

Bacillusspp.

Softdrinks,beers,wines

Saccharomyces

cerevisiae

Enterobacter

spp.


Aminopeptidase

Trichodermareesei

or

longibrachiatum

Aspergillusspp.

Cheese,egg,meats,milk,spices

andflavours

α-A

mylase


Bacillusspp.

Bakeryproducts,softdrinks,beers,wines,cereal

andstarch

processing

Thermoactinomyces

spp.

Bakeryproducts

Bacilluslicheniform

isBacillusspp.

Softdrinks,beers,wines,cereal

andstarch

processing,sugar

andhoney

processing

Arabinofuranosidase

Aspergillusniger

Aspergillusspp.

Catalase

Aspergillusniger

Aspergillusspp.

Cellulase

Trichodermareesei

or

longibrachiatum

Trichodermaspp.


Cyclodextrin

glucanotransferase

Bacilluslicheniform

isThermoanaerobacter

spp.

Cerealandstarch

processing

α-G

alactosidase

Saccharomyces

cerevisiae

Guar

plant


β-Glucanase


Bacillusspp.


Trichodermareesei

or

longibrachiatum

Trichodermaspp.

Cerealandstarch

processing

Glucoam

ylase

or

amyloglucosidase

Aspergillusniger

Aspergillusspp.

Softdrinks,beers,wines,fruitsandvegetables,

cereal

andstarch

processing

Talaromyces

spp.

Cerealandstarch

processing

(Continued)

B.3

Enzymesfrom

geneticallymodified(GM)microorganisms

Table

B3liststheenzymes

from

GM

microorganismsthat

areusedin

foodprocessing.

Table

B3(C

ontinued)

Enzyme

Host

organism

Donororganism

Application

Glucose

isomerase

Streptomyces

lividans

Actinoplanes

spp.

Cerealandstarch

processing

Streptomyces

rubiginosus

Streptomyces

spp.

Cerealandstarch

processing

Glucose

oxidase

Aspergillusniger

Aspergillusspp.

Bakeryproducts,cheese,egg,milk

Aspergillusoryzae

Aspergillusspp.

Bakeryproducts

Hem

icellulase


Bacillusspp.

Bakeryproducts,cereal

andstarch

processing

Hexose

oxidase

Hansenula

polymorpha

Chordrusspp.

Bakeryproducts,cheese,fatsandoils,milk,soups

andbroths,cereal

andstarch

processing

Inulase

Aspergillusoryzae

Aspergillusspp.

Cerealandstarch

processing

Laccase

Aspergillusoryzae

Myceliopthora

spp.


Polyporusspp.


Lactase

or

β-galactosidase

Aspergillusoryzae

Aspergillusspp.

Cheese,dietary

foods,edible

ice,milk

Kluyveromyces

lactis

Kluyveromyces

spp.

Edible

ice,milk

Lipase

triaclyglycerol

Aspergillusoryzae

Candidaspp.

Fatsandoils

Fusarium

spp.

Bakeryproducts,fatsandoils

Rhizomucorspp.

Cheese,fatsandoils,spices

andflavours

Thermomyces

spp.


Lipoxygenase

Escherichia

coli

Pea

Bakeryproducts,spices

andflavours

Maltogenic

amylase


Bacillusspp.


andstarch

processing

Endo-1,4-beta-

mannanase

Trichodermareesei

or

longibrachiatum

Trichodermaspp.

Cerealandstarch

processing

Pectinlyase

Aspergillusniger

var.awamori

Aspergillusspp.

Softdrinks,beers,wines,cocoa,chocolate,coffee

andtea,fruitsandvegetables

Aspergillusniger

Aspergillusspp.

Softdrinks,beers,wines,fruitsandvegetables

Trichodermareesei

or

longibrachiatum

Aspergillusspp.



Pectinmethyl-

esterase

or

pectinesterase

Aspergillusniger

Aspergillusspp.



Aspergillusoryzae

Aspergillusspp.

Softdrinks,beers,wines,fruitsandvegetables

Trichodermareesei

or

longibrachiatum

Aspergillusspp.



Pentosanase


Bacillusspp.

Bakeryproducts

PhospholipaseA

Aspergillusoryzae

Fusarium

spp.

Bakeryproducts

Trichodermareesei

or

longibrachiatum

Aspergillusspp.


PhospholipaseB

Trichodermareesei

or

longibrachiatum

Aspergillusspp.


andstarch

processing

Polygalacturonaseor

pectinase

Aspergillusniger

Aspergillusspp.



Trichodermareesei

or

longibrachiatum

Aspergillusspp.



Protease(incl.milk-

clottingenzymes)

Aspergillusniger

var.awamori

Calfstomach

Cheese

Aspergillusoryzae

Rhizomucorspp.

Cheese,meat

Bacillusamyloliquefaciensor

subtilis

Bacillusspp.

Bakeryproducts,softdrinks,beers,wines,cheese,

fish,meat,milk,cereal

andstarch

processing

Bacilluslicheniform

isBacillusspp.

Fish,meat

Cryphonectria

orEndothia

parasitica

Cryphonectria

spp.

Cheese

Kluyveromyces

lactis

Calfstomach

Cheese

(Continued)

Table

B3(C

ontinued)

Enzyme

Host

organism

Donororganism

Application

Pullulanase

Bacilluslicheniform

isBacillusspp.

Cerealandstarch

processing

Bacillussubtilis

Bacillusspp.


andstarch

processing

Klebsiella

planticola

Klebsiella

spp.


andstarch

processing

Trichodermareesei

or

longibrachiatum

Horm

oconisspp.

Bakeryproducts

Xylanase

Aspergillusniger

Aspergillusspp.

Bakeryproducts,softdrinks,beers,wines

Aspergillusniger

var.awamori

Aspergillusspp.

Bakeryproducts

Aspergillusoryzae

Aspergillusspp.

Cerealandstarch

processing

Thermomyces

spp.

Bakeryproducts


Bacillusspp.

Bakeryproducts,softdrinks,beers,wines,cereal

andstarch

processing

Bacilluslicheniform

isBacillusspp.

Cerealandstarch

processing

Trichodermareesei

or

longibrachiatum

Trichodermaspp.


andstarch

processing

Source:

Adaptedfrom

AMFEP,2015.AMFEPlistofcommercial

enzymes,theAssociationofManufacturers

andForm

ulators

ofEnzymeProducts.Available

at:www.amfep.org/m

ain.

htm

l(lastaccessed

February2016).

Table

B4Examplesoffoodferm

entations

Typeof

ferm

entation

Raw

material

Fermentedfoodsandexamples

ofcountries/areas

Microorganisms

Typicalincubation

conditions

Tem

p(�C)

Tim

e(h)

Lacticacid

Cabbage,

radish,red

peppers

Sauerkraut(Europe,USA),kim

chi

(Korea)

Leuconostocmesenteroides,

Lactobacillusbrevis,L.plantarum

Vegetables,

cucumber,

olive,

mango,

lime

Pickles(M

iddle

East,Europe,USA,

India,Korea,Thailand,China)

Lactobacillusmesenteroides,L.brevis,

L.plantarum,Penecillium

cerevisiae

Amba

48�2

60

Milk

Yoghurt

(worldwide)

Streptococcusthermophilus,

Lactobacillusbulgaricus

40�4

52�3

Fermentedmilksandcreams(e.g.kefir

(Russia),liban

(Iraq),dahi(India),

laban

(Egypt))

Lactococcuslactissubspp.crem

oris,

Lactococcuslactissspp.Lactis,

Acetobacter

orientalis,Lactobacillus

acidophilus,L.delbruecki

sspp.

bulgaricus,L.salivarius

Cheeses(W

estern

world)

Streptococcuscrem

oris,S.diacetylactis,

S.lactis,Penecillium

spp.

32

14�1

6b

Milk/wheat

Kishk(Egypt),trahanas

(Greece,

Turkey)

Tubers(e.g.

cassava)

Kenkey

(Ghana),gari(N

igeria),pozol

(Mexico)

Corynebacterium

spp.,Geotrichum

spp.

Amb

96

(Continued)

B.4

Foodferm

entations

Table

B4describes

somecommonfoodferm

entations.

Table

B4(C

ontinued)

Typeof

ferm

entation

Raw

material

Fermentedfoodsandexamples

ofcountries/areas

Microorganisms

Typicalincubation

conditions

Tem

p(�C)

Tim

e(h)

Rice/shrimps

Balao

balao,burongdalag

(Philippines)

Bacilluspumilus,B.licheniform

isAmb

24�7

2

Wheat,rice,

maize,

lentils

Sourdoughbreads(W

estern

world),idli

(India),hoppers(SriLanka)

injera

(Ethiopia),kisra

(Sudan),puto

(Philippines)

Leuconostocmesenteroides,

Streptococcusfaecalis

Maize

Nonalcoholicbeverages

(e.g.mahew

u

(SouthernAfrica))

L.delbrueckii

45

Meat

Fermentedsausage(W

estern

world,

Thailand)

Pediococcuscerevisiae,Lactobacillus

plantarum,L.curvatus

15�2

624

Aceticacid

Wines,

coconut

water

Vinegars(W

estern

world),kombucha

(Europe,Indonesia,Japan),natade

coco

(Philippines)

Acetobacter

aceti

25

72�1

20

Alcoholic

Grapes,other

fruits,

honey,

palm

sap,

sugarcane,

rice

Wines

(worldwideexceptMuslim

countries)

Saccharomyces

cerevisiae,S.cerevisiae

var.ellipsoideus,S.carbajali,S.

oviform

is,S.chevalieri,

Saccharomycopsisfibuliger,

Kloeckera

apiculata,Zym

omonas

mobilis,Amylomyces

rouxii,S.sake,

Zym

omonasspp.

22�3

0100�3

60c

Cereals(e.g.

rice,maize)

Beers

(worldwideexceptMuslim

countries)

Saccharomyces

cerevisiae(topyeast),S.

carlesbergensis(bottom

yeast),

Leuconostocmesenteroides

20

120�2

40

12�1

5

Wheatand

other

cereals

Leavened

breads(W

estern

countries,

Middle

East)

26

0.5�1

Mixed

(lactic

acid

and/

oryeasts/

moulds)

Fish,

soybeans

Fishsauces(e.g.nuocm

am(V

ietnam

),

shoyuandmiso(Japan),patis

(Philippines),budu(M

alaysia)),and

pastes(e.g.bagoong(Philippines),

belachan

(Malaysia),mam

(Vietnam

),prahoc(Cam

bodia)and

soysauce

(China))

1ststage:

Aspergillusoryzae,A.soyae,

Mucorspp.,Rhizopusspp.

30

48�7

2

2ndstage:

Pediococcussoyae,

Saccharomyces

rouxii

15�2

53�6 m

onths

Cheese

Roquefort,Stilton,Gorgonzola

Penicillium

roquefort

Penecillium

notatum

Cassava,rice

Tape(Indonesia)

Amylomyces

rouxii

Koji(Japan),citric

acid

Aspergillusoryzae

Soybeans

Texturedproducts�

tempeh

(Indonesia)

Rhizopusoligosporus

Cocoabeans

Cocoa(W

estAfrica,South

America)

Lactobacillusplantarum,L.mali,L.

ferm

entum,L.collinoides,

Acetobacter

rancens,A.aceti,A.

oxydans

Amb

144

Coffee

beans

Coffee

(EastAfrica,South

Asia,South

America)

Leuconostocsp.,Lactobacillusspp.,

Bacillusspp.,Erw

inia

spp.,

Aspergillusspp.,Fusarium

spp.

Amb

20�1

00

Alkaline

Locustbean,

melon

seeds,

sesame

seeds,

castor

beans

Daw

adaw

a,iru,ogiri(W

estAfrica),

kenim

a(India),natto

(Japan)

Bacillussubtilis

Amb

aAmbient.

bFermentationofripened

cheesescontinues

for1�1

2months.

cWines

arealso

aged

from

1�5

years.

Source:

Adaptedfrom

thedataofSteinkraus,K.H.,2002.Fermentationsin

worldfoodprocessing.Compr.Rev.FoodSci.FoodSaf.1(1),23�3

2;Raimbault,M.,1998.General

andmicrobiological

aspectsofsolidsubstrate

ferm

entation.Electron.J.Biotechnol.1(3),174�1

88.Available

at:www.scielo.cl/pdf/ejb/v1n3/a09.pdf(lastaccessed

February2016).

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Documents

Annex B: Micro-organisms · There are two types of food poisoning caused by B. cereus: (1) nausea and vomiting similar to symptoms of St. aureus poisoning caused by an emetic toxin