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17: 85–99.

Food Poisoning

P E Granum, The Norwegian School of Veterinary

Science, Oslo, Norway

Background

0001 There are several Bacillus species that have been

involved in food poisoning (Table 1) although the

only species that frequently causes problems is

Bacillus cereus. There are six species that belong to

the B. cereus group including B. anthracis. All of

these species can cause food poisoning and in most

cases are not distinguished in routine food laborator-

ies, apart for B. anthracis, which is usually not hemo-

lytic and is sensitive to penicillin. It has also been

suggested that these species are so closely related

that they should be considered as one species. In this

article, the B. cereus group (apart from B. anthracis)

is dealt with mostly as one species, although B. thur-

ingiensis and B. weihenstephanensis are dealt with

separately. B. cereus is a food-poisoning bacterium

of growing concern, although it does not cause the

types of illness that makes newspaper headlines.

However, outbreaks of both the emetic- and the diar-

rheal type have caused some deaths in recent years. In

some countries, where relatively few outbreaks of

campylobacteriosis and salmonellosis are recorded,

a steady increase in B. cereus food poisoning cases

has been observed. As the Norwegian reference

laboratory for the spore-forming food-poisoning

bacteria, we can follow this trend closely. The same

increase in B. cereus outbreaks is probably hidden

behind the usually more serious outbreaks caused by

other bacteria in Europe and the USA. And indeed it

has been reported to be the most important cause of

foodborne disease in The Netherlands, together with

Salmonella spp., in the years between 1985 and 1991.

0002Bacillus cereus is a Gram-positive, spore-forming,

motile, aerobic rod that also grows well anaerobi-

cally. It is a common soil saprophyte and is easily

spread to many types of foods, especially of plant

origin, but is also frequently isolated from meat,

eggs, and dairy products. B. cereus and other

members of the B. cereus group can cause two differ-

ent types of food poisoning: the diarrheal type and the

emetic type. The diarrheal type of food poisoning is

caused by complex enterotoxins produced during

vegetative growth of B. cereus in the small intestine,

whereas the emetic toxin is preformed during the

growth of cells in the food. For both types of food

poisoning, the food involved has usually been heat-

treated, and the surviving spores are the source of the

food poisoning. B. cereus is not a competitive micro-

organism but grows well after cooking and cooling

(< 42–50



C). The heat treatment will cause spore

germination, and in the absence of competing flora,

B. cereus grows well. Invasion by psychrotolerant

strains from the B. cereus group in the dairy industry

has led to increasing surveillance of B. cereus in recent

years.

0003B. cereus food poisoning is a nonreportable disease

in all of Europe and the USA. Because of this, and

because it is usually a relatively mild and short lasting

tbl0001Table 1 DifferentBacillusspeciesinvolvedinfoodpoisoning

Species

B. c e re us Frequently involved in food poisoning

B. anthracis Has caused food poisoning (see text)

B. thuringiensis Involved in food poisoning

B. mycoides Might have been

involved in food poisoning

B. weihenstephanensis Might have been involved in

food poisoning

B. pseudomycoides Might have been involved in

food poisoning

B. brevis Involved in food poisoning

B. cir culan s Probably not involved, but

has been shown to produce

B. c e re us -type enterotoxin

B. lic heniformis Involved in food poisoning

B. p umilus Involved in food poisoning

B. sphaericus Involved in food poisoning

B. subtilis Involved in food poisoning

The first six species belong to the B. ce reus group and are very closely

related.

BACILLUS

/Food Poisoning 365

disease (< 24 h), it is highly underreported in official

statistics. However, occasional reports have described

more severe forms of the diarrheal type of B. cereus

food poisoning, including a necrotic enteritis type

causing three deaths. A Swiss boy also died after

eating spaghetti containing large amounts of emetic

toxin a few years ago.

0004 The closely related B. thuringiensis is reported to

produce enterotoxins and has been shown to cause

food-poisoning symptoms when given to human vol-

unteers. It has also been reported to cause food

poisoning in regular outbreaks. The extensive use of

this organism as a protective agent against insect

attacks on crops may be part of the increasing prob-

lems with organisms of the B. cereus group observed

in the food industry. Normal procedures for confirm-

ation of B. cereus would not differentiate between the

two species, if at all possible from heat-treated food

products, since B. thuringiensis frequently will throw

out insecticidal plasmids when grown above 30



This makes it difficult to investigate the real numbers

of food-poisoning cases caused by commercially used

B. thuringiensis. To assure safe spraying with B. thur-

ingiensis, the organism in use should be unable to

produce food-poisoning toxins. The Health &

Consumer Protection Directorate-General (European

Commission) has already accepted that only non-

toxin-producing Bacillus spp. should be allowed to

be used in animal nutrition. B. weihenstephanensis

is the psychrotolerant species within the B. cereus

group, and most of the strains of this species are

non- or low toxin producers, although there are ex-

ceptions. There are also B. cereus strains that are able

to grow temperatures as low as 4



0005 The other Bacillus species that might cause food

poisoning are all isolated from soil and foods. How-

ever, in contrast to the members of the B. cereus

group, only a small number of isolates of these species

have the ability to produce toxins (harboring toxin

genes) that can result in food poisoning.

Taxonomy of the

B. cereus

Group

0006 The aerobic endosperm forming bacteria have trad-

itionally been placed in the genus Bacillus. Over the

past three decades, this genus has expanded to accom-

modate more than 100 species. Analysis of 16S ribo-

somal RNA sequences from numerous Bacillus

species has indicated that the genus Bacillus should

be divided into at least five genera or rRNA groups.

The species treated in this text (Table 1) do all still

belong to the genus Bacillus.

0007 Bacillus anthracis, B. cereus, B. mycoides, B. thur-

ingiensis, and, more recently, B. pseudomycoides and

B. weihenstephanensis comprise the B. cereus group.

These bacteria have highly similar 16S and 23S rRNA

sequences, indicating that they have diverged from a

common evolutionary line relatively recently. Exten-

sive genomic studies of B. cereus and B. thuringiensis

have shown that there is no taxonomic basis for

separate species status. Nevertheless, the name

B. thuringiensis is retained for those strains that

synthesize a crystalline inclusion (Cry protein) or d-

endotoxin that may be highly toxic to insects. The cry

genes are usually located on plasmids, and loss of the

relevant plasmid(s) makes the bacterium indistin-

guishable from B. cereus. It is now clear that most

strains in the B. cereus group, including B. thurin-

giensis, carry enterotoxin genes.

Foodborne Outbreaks Caused by the

B. cereus

Group

0008B. cereus is now well recognized as a food-poisoning

organism. Outbreaks can be divided into two types

according to their symptoms. The diarrheal type is far

more frequent in Europe and the USA, whereas the

emetic type appears more prevalent in Japan. Typical

foods implicated are stews, puddings, sauces, and

flour and rice dishes. When expressed as a proportion

of all reported food poisonings, outbreaks ascribed to

B. cereus seem to be concentrated in Scandinavia and

Canada (10–47% of the total) and less frequent in

Central Europe, UK, USA, and the Far East (1–5% of

the total). Although these differences might partly be

due to different consumer habits, they are also not

comparable, because of dissimilar reporting prac-

tices. Thus, in the Netherlands, in 1991, B. cereus

was responsible in 27% of outbreaks in which the

causative agent was identified. However, the inci-

dence was only 2.8% of the total, since the majority

of cases of food poisoning were of unknown etiology.

In addition, when the number of food poisoning cases

ascribed to B. cereus are expressed on a per capita

basis, many of the large regional differences in

incidence disappear. Examples of foods involved in

different outbreaks are listed in Table 2.

Characteristics of the

B. cereus

Disease

0009The emetic toxin results in vomiting, and the second

type, caused by enterotoxins, leads to diarrhea. In a

small number of cases, both types of symptoms are

recorded, probably due to ingestion of preformed

emetic toxin together with living B. cereus cells that

may produce enterotoxins in the small intestine.

There has been some debate about whether or not

the enterotoxin(s) can be preformed in foods and

cause intoxication. From a review of the literature,

it is clear that the incubation time is slightly too long

366

BACILLUS

/Food Poisoning

for that (> 6 h; average 12 h), and in model experi-

ments, it has been shown that the enterotoxins are

degraded on the way to the ileum. Although the

enterotoxin(s) can be preformed, the number of B.

cereus cells in the food would need to be at least

two orders of magnitude higher than that necessary

to cause food poisoning, and such products would no

longer be acceptable to the consumer. The character-

istics of B. cereus food poisoning are listed in Table 3.

0010 In recent years, food poisoning resulting from

ingestion of B. anthracis-infected meat has been

reported in three continents (Asia, Africa, and Amer-

ica). Patients who do not develop anthrax symptoms

instead develop diarrhea, sometimes bloody, with

fever and rashes. It is not yet known whether the

enterotoxins known from B. cereus are at least partly

involved in such symptoms. However, it is known

that enterotoxin genes (nhe) are present in B. anthra-

cis (from the total genome sequence), although the

positive regulator for enterotoxin production (see

Table 4) is nonfunctional, but in other strains, this

might not be the case.

Infectious Dose of

B. cereus

Group

0011Counts ranging from 10

to 10

per gram (or milli-

liter) B. cereus have been reported in affected foods

after food poisoning, giving total infective doses of

about 5 10

–10

. The variation in the infective

dose is partly due to the differences in the amount of

enterotoxin produced by different strains (at least two

orders of magnitude) and partly due to the difference

in infective dose between vegetative cells and spores,

since all the spores will survive the stomach-acid

barrier. Thus, any food containing more than 10

B. cereus per gram cannot be considered completely

safe for consumption.

Virulence Factors/Mechanisms of

Pathogenicity

0012Very different types of toxins cause the two types of

B. cereus food poisoning. The emetic toxin, causing

vomiting, is a ring-formed small peptide, whereas

the diarrheal disease is caused by several different

enterotoxins (Table 4).

Emetic toxin

0013The emetic toxin causes emesis (vomiting) only, and

for many years, its structure was a mystery, as the only

detection system involved living primates. The dis-

covery that the toxin could be detected (vacuolation

activity) by the use of HEp-2 cells led to its isolation

and structural determination. The emetic toxin has

been named cereulide, and consists of a ring structure

tbl0002 Table 2 Examples of the variety of foods involved in Bacillus

cereus food poisoning

Type of food Country Number of

people involved

Type of

syndrome

Barbecued chicken Many countries E, D

Cooked noodles Spain 13 D

Cream cake Norway 5 D

Fish soup Norway 20 D

Lobster pa

UK D

Meat loaf USA D

Meat with rice Denmark > 200 D

Milk Many countries E, D

Pea soup The Netherlands D

Sausages Ireland, China D

School lunch Japan 1877 E

Scrambled egg Norway 12 D

Several rice dishes Many countries E, D

Stew Norway 152 D

Turkey UK, USA D

Vanilla sauce Norway > 200 D

Wheat flour dessert Bulgaria D

E, emetic syndrome; D, diarrheal syndrome.

tbl0003 Table 3 Characteristics of the two types of disease caused by Bacillus cereus

Diarrheal syndrome Emetic syndrome

Infective dose 10

–10

(total) 10

–10

(cells per gram food

to produce enough emetic toxin)

Toxin produced In the small intestine of the host Preformed in foods

Type of toxin Protein(s) Cyclic peptide

Incubation period 8–16 h (occasionally > 24 h) 0.5–5 h

Duration of illness 12–24 h (occasionally several days) 6–24 h

Symptoms Abdominal pain, watery diarrhea

(occasionally bloody diarrhea)

sometimes with nausea

Nausea, vomiting, and

malaise (sometimes followed by

diarrhea, due to additional

enterotoxin production?)

Foods most

frequently implicated

Meat products, soups, vegetables,

puddings/sauces and milk/milk

products

Fried and cooked rice,

pasta, pastry, and noodles

BACILLUS

/Food Poisoning 367

of three repeats of four amino-and/or oxy-acids:

[d-O-Leu-d-Ala-l-O-Val-l-Val]

. This ring structure

(dodecadepsipeptide) has a molecular mass of

1.2 kDa and is chemically closely related to the potas-

sium ionophore valinomycin. The emetic toxin is re-

sistant to heat, pH, and proteolysis, but is not

antigenic. The biosynthetic pathway and mechanism

of action of the emetic toxin still have to be eluci-

dated, although it has been shown recently that

it stimulates the vagus afferent through binding to

the 5-HT

receptor. It has just been shown that

cereulide is synthesized non-ribosomally by a peptide

synthetase.

0014 Cereulide was responsible for the death (fulminant

liver failure) of a 17-year-old Swiss boy a few years

ago. A large amount of B. cereus emetic toxin was

found in the residue from the pan used to reheat the

food (pasta) and in the boy’s liver and bile. In a recent

experiment, mice were injected i.p. with synthetic

cereulide, and the development of histopathological

changes was examined. At high cereulide doses, mas-

sive degeneration of hepatocytes occurred. The serum

values of hepatic enzymes were highest on days 2–3

after the inoculation of cereulide, and rapidly de-

creased thereafter. General recovery from the patho-

logical changes and regeneration of hepatocytes was

observed after 4 weeks.

Enterotoxins

0015 As shown in Table 4, three different enterotoxins,

believed to be involved in food poisoning, have been

characterized to date. The three-component hemoly-

sin (Hbl; consisting of three proteins: B, L

, and L

)

with enterotoxin activity was the first to be fully

characterized. This toxin also has dermonecrotic

and vascular permeability activities, and causes fluid

accumulation in ligated rabbit ileal loops. Hbl has

been suggested to be a primary virulence factor in

B. cereus diarrhea. Convincing evidence has shown

that all three components are necessary for maximal

enterotoxin activity. It has been suggested, from

studies of interactions with erythrocytes, that the B

protein (HblA) is the component that binds Hbl to the

target cells, and that L

(HblD) and L

(HblC) have

lytic functions. More recently, another model for the

action of Hbl has been proposed, suggesting that

the components of Hbl bind to target cells independ-

ently and then constitute a membrane attacking com-

plex, resulting in a colloid osmotic lysis mechanism.

Substantial heterogeneity has been observed in the

components of Hbl, and individual strains have been

shown to produce various combinations of single or

multiple bands of each component.

0016More recently, a nonhemolytic three-component

enterotoxin (Nhe) has been characterized. The three

components of this toxin are different from the com-

ponents of Hbl, although there are similarities. The

three components of Nhe enterotoxin were first

purified from a B. cereus strain isolated after a large

food-poisoning outbreak in Norway in 1995. Binary

combination of the components of this enterotoxin

shows some biological activity, but not nearly as high

as when all the components are present.

0017Almost all tested B. cereus/B. thuringiensis strains

produce Nhe, and about 60% produce Hbl. At pre-

sent, we do not know how important each of them is

in relation to food poisoning. There are several food-

poisoning strains that do not produce Hbl, but none

that do not produce Nhe.

0018The newly discovered cytotoxin K (CytK) is similar

to the b-toxin of Clostridium perfringens (and other

related toxins) and was the cause of the symptoms in a

severe outbreak of B. cereus food poisoning in France

in 1998. In this outbreak, several people developed

bloody diarrhea, and three died. This could be con-

sidered an outbreak of B. cereus necrotic enteritis,

although it is not nearly as severe as the C. perfringens

type C food poisoning.

0019There is significant sequence identity between the

three proteins of Nhe and between the Nhe and Hbl

proteins. The identity is highest in the N-terminal

third of the proteins. The most pronounced gene

tbl0004 Table 4 Toxins involved in food poisoning produced by Bacillus cereus

Toxin Type/size Foodpoisoning

Hemolysin BL (Hbl) Protein, three components transcribed

from one operon: HblC (L

-component),

HblD (L

-component) and HblA

(B-component); the proteins have

a molecular mass of 37–46 kDa

Probably

Nonhemolytic

enterotoxin (Nhe)

Protein, three components transcribed

from one operon: NheA, NheB, and

NheC; the proteins have a molecular

mass of 36–41 kDa

Yes

Cytotoxin K (CytK) Protein, one component, 34 kDa Yes, three deaths

Emetic toxin (cereulide) Cyclic peptide, 1.2 kDa Yes, one death

368

BACILLUS

/Food Poisoning

sequence similarities are found between nheA and

hblC, nheB and hblD, and nheC and hblA. This is

not only in direct comparison of the sequences, but

also in predicted transmembrane helices for the six

proteins. NheA and HblC have no predicted trans-

membrane helices, whereas NheB and HblD have two

each. Finally, NheC and HblA have one predicted

transmembrane helix each, in the same position in

the two proteins. Although there are some similarities

among the components of Hbl and Nhe, they cannot

be substituted for each other to give biological active

complexes.

Other Possible Virulence Factors

0020 The B. cereus spore is more hydrophobic than any of

the other Bacillus spp. spores, which makes it adhe-

sive to several types of surfaces. This makes it difficult

to remove during cleaning and a difficult target for

disinfection. The B. cereus spores also contain ap-

pendages and/or philli that are, at least partly, in-

volved in adhesion (Figure 1). These properties of

the B. cereus spore not only allow them to survive

sanitation, and thus become available for contamin-

ation of different foods, but also aid adherence to

epithelial cells. Experiments have shown that spores,

at least from one strain isolated after one outbreak,

can indeed adhere to Caco-2 cells in culture and that

these properties are linked to hydrophobicity and

possibly to the appendages. A longer incubation

period is observed in this case, as expected, as the

spore would first have to germinate.

Commercial Methods for Detection of the

Bacillus

cereus

Toxins

0021 Neither of the two available commercial immuno-

assays can quantify the toxicity of the enterotoxins

from B. cereus. The assay from Oxoid measures the

presence of the HblC (L

) component, whereas

the Tecra kit mainly detects the NheA protein. How-

ever, if one or both of the commercial kits react

positively with proteins from B. cereus supernatants,

it is likely that the strain is enterotoxin-positive, spe-

cifically if the strains are cytotoxic on epithelial cells.

If the supernatants are shown to be cytotoxic, the

strains can be regarded as enterotoxin-positive. At

present, there is no commercial method available

to detect CytK, and, unfortunately, no commercial

method to detect the emetic toxin either. However, a

specific, sensitive, semiautomated, and quantitative

Hep-2 cell culture-based 3-(4,5-dimethylthiazol-2-

yl)-2,5-diphenyltetrazolium bromide assay for B. cer-

eus emetic toxin has been developed.

Other Bacillus Species

0022Of the other Bacillus species involved in food

poisoning, only three have been involved frequently

enough to give a relatively clear picture of the diverse

food-poisoning symptoms (Table 5). For B. sphaeri-

cus and B. brevis, only a few cases have been

recorded. The infective dose variation for these

species is not clear, although they are probably quite

high (> 10

). From the data in Table 5, it is clear that

many types of toxins are involved. For incubation

periods shorter than 6 h, preformed toxins are

expected. Enterotoxins similar to those of B. cereus

have been detected from several of the other Bacillus

species (Table 1) using immunological methods and

polymerase chain reaction-based methods. However,

until the toxins have been isolated and characterized,

there structure and function are mostly speculative.

0023One of the toxins has been well characterized.

From a strain of B. licheniformis isolated for milk

powder (which caused the death of a young child), a

toxin similar to the B. cereus emetic toxin was isol-

ated. This toxin was also found in 13 out of 210

isolates (6%) of B. licheniformis from different

sources (mainly from foods). The toxins isolated

from three strains of different origins contained the

same component each of which had the same amino

acid residues l-Gln, l-Leu, d-Leu, l-Val, l-Asp,

d-Leu, and l-Ile, in that order. Toxins were identified

as lichenysin A, a cyclic lactonic heptalipopeptide in

which the main 3-hydroxy fatty acids are 13–15

carbons in length. The molecular mass of this toxin

is about 1 kDa.

Prevention and Control of

Bacillus

Food

Poisoning

0024Prevention and control of Bacillus spp. is relatively

easy, apart from in the dairy industry, where B. cereus

Appendages

Exosporium

Coat

Cortex

Core

fig0001 Figure 1 Bacillus cereus spore with the different layers and

appendages.

BACILLUS

/Food Poisoning 369

causes major problems. There are also a growing

number of precooked long-life products on the

market that are difficult to produce completely free

from Bacillus spp. spores. The growth characteristics

of the four most common food-poisoning Bacillus

spp. are listed in Table 6. If foods are not kept at

6–60



C for too long, no spore germination and

growth of these species will occur. Rapid cooling

and proper reheating of cooked food are essential if

the food is not consumed immediately. Long-term

storage must be at temperatures below 8



C (or pref-

erably 4–6



C to prevent growth of B. cereus). Low-

pH foods (pH 4.3) can be considered safe from

growth of the food-poisoning Bacillus spp. Bacillus

spores are commonly isolated from spices, cereals,

and dried foods. For example, during 1960–8,

B. cereus was the third most common cause of food

poisoning in Hungary, and meat dishes were

frequently involved. The reason for this was the pref-

erence for well-spiced meat dishes in Hungary. Sev-

eral cases of B. cereus food poisoning, (involving

many people) resulting from consumption of meat-

containing dishes have also been reported recently in

Norway.

0025 The emetic syndrome of B. cereus food poisoning

is often connected with the consumption of rice in

Chinese restaurants. The predominance of cases

in Chinese restaurants is linked with the common

practice of saving portions of boiled rice from bulk

cooking. The boiled rice is then stored, usually at

room temperature, overnight and B. cereus is then

able to multiply. The same problem may occur when

foods such as pasta and pizza are stored for long

periods of time at room temperature.

0026At present, the main problem with B. cereus seems

to be in the dairy industry, where the keeping quality

of milk is determined by the number of B. cereus cells/

spores in the product. The bacterium may cause ag-

gregation of the creamy layer of pasteurized milk,

known as bitty cream, which is explained by the

lecithinase activity of B. cereus. Further, B. cereus is

responsible for sweet curdling (without pH reduc-

tion) in both homogenized and nonhomogenized

low-pasteurized milk. It seems impossible to com-

pletely avoid the presence of B. cereus in milk where

it already infects raw milk at the farm. Soiling of the

udders of cows is the principal source of contamin-

ation of milk with B. cereus. Soil has been shown to

contain 10

–10

spores per gram. It is very important,

therefore, that the udder and the teats are cleaned to

reduce the contamination of raw milk. Transport and

further storage in the dairy may result in further

tbl0005 Table 5 Characteristics of the illness caused by the three Bacillus species other than B. c e re us causing food poisoning

Bacillus subtilis Bacillus licheniformis Bacillus pumilus

Foods involved Meat dishes with elements

of vegetables

Meat dishes with

elements of vegetables

Meat products

Seafood with rice

Sandwiches

Bread and pastry products

Bread and pastry products Canned tomato juice

Sandwiches

Chicken

Pizzas

Infective dose > 10

>10

Incubation period 10 min to 14 h 2–14 h 15 min to 11 h

Duration 2–8 h 6–24 h

Symptoms:

Vomiting 80% 54% Yes

Diarrhea 49% 92% Yes (not all)

Abdominal pain/cramps 27% 46% ?

Other symptoms Nausea, headaches,

and flushing/sweating

Not reported Not reported

tbl0006 Table 6 Factors determining the growth of the four most common food-poisoning Bacillus species

Species pHrange Temperaturerange Other factors

Bacillus cereus 4.3–9.3 4–50



C Growth at a

to 0.92

Inhibited by 0.2% sorbic acid (pH < 5.0)

Growth in 7% NaCl

Bacillus subtilis 5.0–8.5 10–50



C Growth in 7% NaCl

Growth with only glucose and ammonium

Bacillus licheniformis 5–? > 15–55



C Growth in 7% NaCl

Bacillus pumilus 5–? 10–45



C Growth in 7% NaCl

370

BACILLUS

/Food Poisoning

contamination of the raw milk from B. cereus spores

already present (adherent) in the tanks or pipelines.

The vegetative bacteria are killed in the pasteuriza-

tion process, but the spores survive. Pasteurization

might activate at least some of the spores (heat acti-

vation), which might start germinating.

0027 To control B. cereus in milk and milk products, it is

very important to trace the presence of spores from

farmer to package. The storage temperature is the

most important factor in keeping B. cereus numbers

to a minimum. Figure 2 shows the number of days

required before milk contains more than 10

B. cer-

eus per milliliter at different temperatures. An

increase of just 2



C during storage, from 6 to 8



increase the growth rate substantially. At the dairy,

the milk is generally kept at 4



C, thus ensuring a

good keeping quality. However, during distribution,

where the energy costs are often valued higher than

food quality, temperatures up to 8



C and above are

common. Further, the consumer often exposes milk to

higher temperatures for longer periods, for example

at the breakfast table. The majority of the strains

from the B. cereus group that grow at low tempera-

tures (including B. weihenstephanensis) are usually

low in enterotoxin production, although there are

exceptions.

0028 As mentioned before, the spores of B. cereus are

very adhesive to different hydrophobic surfaces (such

as glass and stainless steel), and for this reason,

B. cereus is often found in food plants and kitchen

environments. The strong adhesion of B. cereus

spores is mainly due to three characteristics: the

high relatively hydrophobicity, the low spore surface

charge, and the spore morphology (appendages). At

present, the only way to overcome this problem,

when first introduced, is through the use of hypo-

chlorite (0.2% at pH 7–8) or UVC light, since neither

low- nor high-pH cleaning is sufficient to control the

problem.

See also: Bacillus: Occurrence; Detection; Food

Poisoning: Classification; Statistics

Further Reading

Agata N, Ohta M, Mori M and Isobe M (1995) A novel

dodecadepsipeptide, cereulide, is an emetic toxin of

Bacillus cereus. FEMS Microbiology Letters 129: 17–20.

Andersson A, Granum PE and Ro

nner U (1998) The adhe-

sion of Bacillus cereus spores to epithelial cells might

be an additional virulence mechanism. International

Journal of Food Microbiology 39: 93–99.

Beecher DJ, Schoeni JL and Wong ACL (1995) Enterotoxin

activity of hemolysin BL from Bacillus cereus. Infection

and Immunity 63: 4423–4428.

Drobniewski FA (1993) Bacillus cereus and related species.

Clinical Microbiological Reviews 6: 324–338.

Granum PE (2001) Bacillus cereus. In: Doyle M, Beuchat L

and Montville T (eds) Food Microbiology. Fundamen-

tals and Frontiers, pp. 373–381. Washington, DC: ASM

Press.

Granum PE and Baird-Parker TC (2000) Bacillus spp. In:

Lund B, Baird-Parker T and Gould G (eds) The Micro-

biological Safety and Quality of Food, pp. 1029–1039.

Guithersburg, MD: Aspen.

Granum PE and Brynestad S (1999) Bacterial toxins as

food poisons. In: Alouf JE and Freer JH (eds) The

Comprehensive Sourcebook of Bacterial Protein Toxins,

pp. 669–681. London: Academic Press.

Kramer JM and Gilbert RJ (1989) Bacillus cereus and other

Bacillus species. In: Doyle MP (ed.) Foodborne Bacterial

Pathogens, pp. 21–70. New York: Marcel Dekker.

McKillip JL (2000) Prevalence and expression of entero-

toxins in Bacillus cereus and other Bacillus spp. Antonie

Van Leeuwenhoek 77: 393–399.

Salkinoja-Salonen MS, Vuorio R, Andersson MA et

al.(1999) Toxigenic strains of Bacillus licheniformis re-

lated to food poisoning. Applied and Environmental

Microbiology 65: 4637–4645.

Bacteria See Microbiology: Classification of Microorganisms; Detection of Foodborne Pathogens and their

Toxins; Antibiotic-resistant Bacteria

0123456789101112

100

1000

10 000

100 000

1 000 000

Days after pasteurization

Bacillus cereus cells/ml

9 8

8 8

7 8

6 8

fig0002 Figure 2 Growth rate of Bacillus cereus cells in milk stored at

9, 8, 7, and 6



BACILLUS

/Food Poisoning 371

Baking See Biscuits, Cookies, and Crackers:NatureoftheProducts;MethodsofManufacture;Chemistryof

BiscuitMaking;Wafers; Bread:DoughMixingandTestingOperations;BreadmakingProcesses;Chemistryof

Baking;SourdoughBread;DietaryImportance;DoughFermentation; Cakes:NatureofCakes;Methodsof

Manufacture;ChemistryofBaking

Baking Powder See Leavening Agents

BANANAS AND PLANTAINS

J W Daniells,QueenslandDepartmentofPrimary

Industries,Queensland,Australia

Introduction

000 1 Bananas and plantains (Musa spp.) are grown exten-

sively throughout the tropical and subtropical regions

of the world. Together they represent the number-one

fruit crop in the world, in terms of both production

and trade, exceeding oranges by 37  10

t per year

for production and by 10  10

t per year for trade.

Most of the exported fruit, which makes up only 15%

of the total, are Cavendish-type dessert bananas.

However, bananas and plantains that are cooked ac-

count for almost half of the world production. This

article describes their global distribution and import-

ance, the morphological and nutritional characteris-

tics of the fruit, handling and storage, and other uses

of fresh and processed fruit. (See Fruits of Temperate

Climates: Commercial and Dietary Importance.)

0002 The terms ‘bananas’ and ‘plantains’ require clarifi-

cation. ‘Bananas’ refers to all the members of the

genus Musa. In the narrow sense, plantains are a

defined group within this genus which have the AAB

genome and are characterized by the orange-yellow

color of both the compound tepal of the flower and

the fruit pulp at ripeness. When ripe, a relatively high

proportion of starch (10–25% of fresh weight) is

present in the pulp. The fruits are slender, angular

to pointed, and are generally palatable only after

cooking. Plantains, in the broad sense, include other

members of the genus Musa that are starchy at ripe-

ness but which lack the other characteristics. In this

article, plantains are referred to in the narrow sense,

except when global production figures are discussed,

as these refer to plantains in the broad sense.

Global Distribution

0003Before international trade began a little over 100 years

ago, bananas in temperate regions were merely a curi-

osity. Bananas are grown in commercial plantations,

but more often in household gardens because of their

almost universal appeal as a food, ease of growing,

quick production, and attractive plant appearance.

0004Bananas and plantains are suited to the warm,

high-rainfall regions of the lowland tropics. They

originated in South-east Asia (including Papua New

Guinea) and have been spread to other regions of the

world in the past 2000 years. They are now grown

from the equator to about 35



N and 30



S, and within

these latitudes they may be grown in semiarid loca-

tions with irrigation or in large plastic greenhouses.

0005Bananas for export are produced mainly in Central

and South America as well as the Philippines (Tables

1–4). Most exported fruit goes to North America,

Europe, and Japan, and in 2000 was valued at

$4.306 10

. Exports of plantains have increased in

importance in recent years but still represents less

than 2% of the combined total exports of bananas

and plantains. Other major areas of banana produc-

tion are South-east Asia and East Africa (according to

Food and Agriculture Organization (FAO) statistics*)

but little of this is exported. Plantain production is

most important in East and West Africa as well as

South America.

0006Average world consumption of bananas and plan-

tains in 2001 was about 16 kg per person per year.

However, in much of Africa and Latin America it is

5–10 times this amount, and it is as much as 450 kg

*FAO production statistics need careful interpretation because the

meaning of the words ‘bananas’ and ‘plantains’ differs among

countries, particularly in East Africa. For instance information

from Burundi on bananas largely refers to plantains used for

cooking purposes.

372 BANANAS AND PLANTAINS

per person per year in some parts of East Africa. The

major export production areas are located close to the

equator, where an even supply of fruit throughout

the year is possible, and where they are less damaged

by cyclones or typhoons.

000 7 The optimum temperature range for bananas is

about 22–31



C. Chilling injury of fruit occurs when

the latex coagulates at temperatures below 13



Bananas are susceptible to frost and in subtropical

regions are often planted on hillsides to avoid it.

The growth cycle is greatly prolonged outside the

tropics and productivity is generally reduced. The

industries that have developed in the subtropics

have largely done so because of proximity to markets.

Varieties

0008 All the edible bananas belong to the Eumusa (some-

times referred to as Musa) section of the genus Musa,

except for the Fe’i bananas of the Pacific region which

belong to the Australimusa section (Figure 1). The

Fe’i bananas are characterized by erect bunches and

pink-red sap, and an orange, slimy fruit pulp that

generally requires cooking. There are numerous wild

seeded species in each of the Musa sections.

000 9 Edible bananas and plantains belonging to the

Eumusa section are believed to contain genomes

from two wild species, M. acuminata (A) and M.

balbisiana (B). Most cultivated bananas are trip-

loid and are classified according to characteristics

estimating the contribution of the two parent

species. Because the binomial Latin nomenclature

for edible varieties, e.g., Musa cavendishii cultivar

(cv.) Williams, proved unsatisfactory, they are re-

ferred to as, for example, Musa spp. (AAA Group,

Cavendish Subgroup) cv. Williams. There are about

tbl0002Table 2 Proportionofworldproductionof29milliontonnesof

plantainsamongregionsandcountries2001

RegionCountry

Percentageof

totalworld

production

(2910

Asia3.9

SouthAmericaColombia9.7

Peru5.0

Venezuela2.4

Ecuador1.6

Other0.8

CentralAmericaDominicanRepublic1.2

Cuba1.3

Other3.5

AfricaUganda32.7

Rwanda5.4

CongoDemocraticRepublic1.8

Ghana6.6

Nigeria6.5

IvoryCoast5.2

Cameroon4.8

Tanzania2.2

Other5.4

Source:FoodandAgricultureOrganization20August2002:www.fao.org.

tbl00 01 Table 1 Proportionofworldproductionof69milliontonnesof

bananasamongregionsandcountries2001

RegionCountry

Percentageoftotalworld

production(6910

AsiaIndia23.3

China7.9

Philippines7.4

Indonesia5.2

Thailand2.5

Vietnam1.6

Other2.8

SouthAmericaBrazil8.4

Ecuador11.0

Colombia2.0

Other3.0

CentralAmericaCostaRica3.3

Mexico2.9

Honduras0.7

Guatemala1.1

Panama0.7

Other0.4

AfricaBurundi2.3

Cameroon1.2

Uganda1.4

Other6.3

Other4.6

Source:FoodandAgricultureOrganization20August2002:www.fao.org.

tbl0003Table 3 Proportionofworldexportsof14milliontonnesof

bananasamongregionsandcountries2000

RegionCountry

Percentageoftotalworld

exports(1410

AsiaPhilippines11.2

Other1.2

SouthAmericaEcuador28.1

Colombia12.0

Other1.0

CentralAmericaCostaRica14.7

Guatemala5.6

Honduras1.3

Panama3.4

Other1.3

Africa2.9

Other17.3

Source:FoodandAgricultureOrganization20August2002:www.fao.org.

BANANAS AND PLANTAINS 373

500 varieties of bananas and plantains in existence,

but only 150 or so are primary clones and the remain-

der are somatic mutants.

0010 Bananas for export now come almost entirely from

varieties of the Cavendish subgroup. From the 1940s

to 1960s, these replaced cv. Gros Michel, which was

devastated by a soil-borne fungus called Panama

disease (fusarium wilt) in one of the largest disease

epiphytotics that has ever occurred in crop plants.

The greatest diversity of varieties occurs in South-

east Asia where particular varieties are especially

favored for various culinary uses (Figure 2).

0011The leaf disease, black Sigatoka, and new races of

Panama disease currently pose major threats to world

banana and plantain production. As resistant var-

ieties are developed by conventional breeding pro-

grams, somacloning and genetic engineering, further

changes in the varieties cultivated can be expected.

Fruit Morphology and Anatomy

0012The banana plant is a large, tree-like, determinate

perennial herb with a basal rhizome, a pseudostem

composed of leaf sheaths, and a terminal crown of

large leaves (Figure 3). The terminal inflorescence is

initiated near ground level and is then thrust up

the center of the pseudostem by elongation of the

true stem. The basal flower clusters (hands) are

female and form the fruit bunch. Distal flower clus-

ters are male, do not produce fruit, and are commonly

deciduous. The banana has the largest inflorescence

of any plant grown as a crop. The world record for a

mature fruit bunch is 144 kg, obtained in the Canary

Islands.

0013Banana bunches have from one to 20 hands and

take 2–6 months to reach maturity. Bunches are pen-

dant or subhorizontal and usually weigh between 10

tbl0004 Table 4 Proportionofworldimportsof14milliontonnesof

bananasamongregionsandcountries2000

RegionCountry

Percentageoftotalworld

imports (14 10

Asia Japan 7.6

China 4.2

Other 5.8

North America USA 28.2

Canada 2.8

Europe Germany 7.8

Belgium 7.2

UK 5.2

Italy 4.2

Russian Federation 3.5

France 2.4

Poland 2.0

Other 12.5

Other 6.6

Source:FoodandAgricultureOrganization20August2002:www.fao.org.

Family Musaceae

Genus Ensete Musa

Section Australimusa Callimusa Rhodochlamys Eumusa Ingentimusa

Genome AA AAA AAAA /AAAB /AABB AB AAB ABB

Subgroup/

cultivar

Fe’i Sucrier

Lakatan

Gros Michel

Red

Cavendish

Yangambi km5

East African

Highland bananas

Breeding

program

selections

Ney Poovan Pisang Raja

Pisang Kelat

Mysore

Pome

Plantain

Maia Maoli/Popoulu

Silk

Iholena

Bluggoe

Pisang Awak

Saba

Ney Mannan

Kluai Teparot

fig0001 Figure 1 Systematic position of banana varieties.

Considered as BBB in the Philippines. Modified from Stover and Simmonds

(1987).

374 BANANAS AND PLANTAINS