Caballero B. (ed.) Encyclopaedia of Food Science, Food Technology and Nutrition. Ten-Volume Set

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and equipment. (See Beers: Biochemistry of Fermen-

tation; Chemistry of Brewing.)

0050 All equipment is usually in type 304 stainless steel,

the corrosion resistance of which is well suited to the

product and to the solutions used as cleaning agents.

As mentioned previously, some precautions must

nevertheless be taken when using chlorine-containing

cleaning solutions, and the cleaning instructions given

by equipment fabricators must be strictly observed.

Type 316 stainless steel is used for brewing equipment

when the chloride content of available water is

particularly high (Figure 3).

0051 Practically all new beer barrels are now fabricated

in stainless steel in substitution of aluminum barrels

which, as a consequence, play a declining part in beer

storage and transportation. Stainless steel barrels,

fabricated from two deep-drawn half-shells of

type 304 stainless steel welded together, are price-

competitive and bring decisive advantages: high

strength, easy cleaning and disinfection and limited

maintenance while maintaining a similar weight

(Figure 4). (See Barrels: Wines, Spirits, and Other

Beverages; Beer Making.)

Mineral Water, Soft Drinks, and Fruit Juice

0052 Stainless steel is now in general use for equipment

used in the collection and treatment of mineral waters

as well as for the processing of soft drinks. According

to the type of water and its temperature and, for soft

drinks, the nature of additions, type 304 or type 316

stainless steel is used.

0053 For fruit juices and fruit juice-based drinks, use of

type 316 molybdenum-containing stainless steel is

recommended to avoid any risk of contamination by

iron or copper, which could spoil the taste or destroy

vitamins.

Fruits and Vegetables

0054There is a great diversity of processes for the pre-

paration and treatment of fruit and vegetables and,

as a consequence, a great diversity of processing

equipment. Generally speaking, stainless steel type

304 is used for all surfaces in contact with the product

at any stage of its preparation. Nevertheless, for

some products and, in particular, for treatments

at elevated temperature, it is necessary to call for

molybdenum-containing stainless steel type 316.

In the processing cycle of tomato concentrate, for

instance, evaporators are made from type 316 stain-

less steel.

0055For the storage of virgin olive oil, EC regulations

now specify the use exclusively of type 304 stainless

steel for the fabrication of storage tanks. This is to

avoid any risk of quality alteration during storage.

Owing to the aggressiveness of hot fatty acids, edible

oil refining equipment, operated at elevated tempera-

ture, needs the use of type 316 stainless steel. (See

Vegetable Oils: Oil Production and Processing.)

0056In the beet sugar industry, the use of thin-wall

welded tubes of ferritic or austenitic stainless steel

for the fabrication of evaporators is expanding, in

substitution for carbon steel. It appears the most

economic solution on a lifecycle cost basis. (See

Sugar: Refining of Sugarbeet and Sugarcane.)

Meat Industry

0057Stainless steels are used for the fabrication of virtually

all equipment for slaughtering, preparation, and

fig0002 Figure 2 A battery of wine storage tanks made from chromium nickel molybdenum stainless steel. Addition of molybdenum allows

the tanks to be used for white as well as red wine. (Courtesy of UGINE S.A., France.)

3874 METALS USED IN THE FOOD INDUSTRY

handling of meat. They provide a guarantee of clean-

ability and hygiene. (See Meat: Slaughter.)

0058 Type 304 stainless steel is generally satisfactory,

and its applications range from conveyors, cutting

machines, and work surfaces to easy-clean wall

covering. For the collection and treatment of blood,

however, type 316 molybdenum-containing stainless

steel must be selected for this more aggressive use.

The same grade must also be used for meat salting

plants.

Miscellaneous Food Industry Equipments

0059Stainless steel is used in many food-processing indus-

tries other than those reviewed above. These include

confectionery, chocolate and biscuit manufacture, in-

dustrial bakery, food deep freezing, fish preparation,

and canning. As a general rule, stainless steel is used

at least for parts in contact with foodstuffs but in-

creasingly for the whole equipment of the plant. A

recent tendency is to move to stainless steel for the

fig0003 Figure 3 (see color plate 106) Stainless steel fermentation vessels and associated pipework in a modern brewery. (Courtesy of

Courage Ltd and British Steel plc.)

METALS USED IN THE FOOD INDUSTRY 3875

framework of equipment traditionally made from

painted carbon steel; the advantages of this substitu-

tion are a better cleanability and a lessening of main-

tenance works, which compensate quickly for the

higher initial cost. Refer to individual processes.

0060 Some equipment is used by several food industries,

for example bottling and packing machinery; stain-

less steels are used for parts in direct contact with the

beverages and foodstuffs handled. These include

band or chain conveyors, tanks of filling machines,

cladding of machinery framework and, sometimes, as

mentioned above, also for the supporting framework

itself.

0061 At the end of the food-preparation chain, the prep-

aration of ready cooked dishes and their preservation

by chilling, deep freezing, vacuum packing or can-

ning, and the catering industry with its kitchen and

serving facilities must be mentioned. Stainless steel is

extensively used in equipment for these industries

where cleanability and hygiene are a prime necessity.

See also: Barrels: Wines, Spirits, and Other Beverages;

Beers: Chemistry of Brewing; Biochemistry of

Fermentation; Brandy and Cognac: Armagnac, Brandy,

and Cognac and their Manufacture; Cleaning

Procedures in the Factory: Types of Detergent; Types of

Disinfectant; Contamination of Food; Corrosion

Chemistry; Meat: Slaughter; Milk: Processing of Liquid

Milk; Sugar: Refining of Sugarbeet and Sugarcane;

Vegetable Oils: Oil Production and Processing; Vinegar;

Wines: Production of Table Wines; Production of

Sparkling Wines

Further Reading

Crolet JL, Hooper RAE, Lennartz G and Tytgat G (1975)

Contribution a

l’e

laboration d’une re

glementation des

mate

riaux destine

tre mis en contact avec les denre

et substances alimentaires: cas des aciers inoxydables.

Industries Alimentaires et Agricoles 6: 619–827.

Daufin G and Kerherve L (1990) Le nettoyage des aciers

inoxydables dans l’industrie agroalimentaire. In:

Lacombe P, Baroux B and Beranger G (eds) Les Aciers

Inoxydables, Ch. 23, pp. 839–851. Les Vulis: Les

Editions de Physique.

Di Caprio G (1976) Le applicazioni nell’ industria alimen-

tare. Gli Acciai Inossidabile, Ch. 12, pp. 362–390.

Milan: Ulrico Hoepli.

Henry P, Blouin J, Fourton S, Guimberteau G and Peynaud

E (1972) Sur l’utilisation des aciers inoxydables dans les

installations vinicoles. Connaissance de la Vigne et du

Vin 177–212.

Holah JT and Thorpe RH (1990) Cleanability in relation to

bacterial retention on unused and abraded domestic sink

materials. Journal of Applied Bacteriology 69: 599–608.

Ridenour GM and Armbruster EH (1953) Bacterial clean-

ability of various types of eating surfaces. American

Journal of Public Health 43: 138–149.

fig0004 Figure 4 (see color plate 107) Stainless steel’s hygienic and corrosion resistance properties are vital in the brewing industry. Today,

all new beer barrels are made with type 304 stainless steel. (Courtesy of British Steel plc.)

3876 METALS USED IN THE FOOD INDUSTRY

MICROBIOLOGY

Contents

Classification of Microorganisms

Detection of Foodborne Pathogens and their Toxins

Classification of

Microorganisms

A A A Kwaasi, King Faisal Specialist Hospital &

Research Centre, Riyadh, Saudi Arabia

Background

0001 Microorganisms comprise prokaryotes as well as

some eukaryotic organisms, and these include bac-

teria, fungi, viruses, protozoa, and algae. Food can

be defined as anything that, when taken into the body,

serves to nourish or build up the tissues, or to supply

body heat: essentially, an aliment or nutrient. This

definition of food encompasses all items that are con-

sumed by man and other animals. Water, beverages,

and all edible solid material are food. Food sources

are plankton, seaweed, fish, crustacea, mushrooms,

molluscs, meat, poultry, fruits, vegetables, edible

algae and fungi, as well as grains.

0002 Microbes are in contact with food whether it is on

the farm or in the forest, garden, lake, pond, river, or

sea. Food in storage, industrial processing machines,

supermarkets, warehouses, brewery holdings, res-

taurants, hotels and public dining places all have, at

one stage or another, harbored or been in contact

with microorganisms.

0003 A number of microorganisms are in themselves

food or can be exploited and used as food. Some are

contaminants on food and food products, and a

number can also cause food spoilage or produce

toxins in foods leading to foodborne illnesses in man

and animals. Some microorganisms are also capable

of transforming a food’s properties in a beneficial way

such as the various food fermentation processes. Since

there are a large number of different microorganisms

with diverse habitats and different attributes, food

microorganisms will be classified here in terms of

the way in which they are associated with foods in

different habitats, cause food spoilage, contaminate

food, or harm the consumer by the production of

noxious metabolites. Microorganisms are ubiquitous

and can survive and grow at different temperatures at

which food is either kept or processed. They exist

from the coldest of salty ponds in the frozen wasters

of the polar regions to the boiling water of hot

springs. Actively growing bacteria may occur at tem-

peratures in excess of 100



C in thermal volcanic

vents at the bottom of the deeper parts of the oceans,

in acid wastes from mines, or in alkaline waters of

soda lakes. Microbes have been isolated from black

anaerobic silts of estuarine mud and also have been

found in the purest waters of the biologically unpro-

ductive or oligotrophic lakes. This means that, irre-

spective of the environment, microorganisms can find

a way of adapting, surviving, and multiplying at dif-

ferent temperatures, and they exist in a similar

manner on food.

Microorganisms on Food Crops in the

Farm or Garden

0004Crops are established by sowing seed or planting

vegetatively propagated materials such as tubers,

corms, stem cuttings, or suckers. These vegetative

materials are rich in food reserves and, given suitable

conditions of temperature, moisture, and light, they

are hydrolyzed into simple sugars, which are then

utilized in the early growth of the rudimentary

young plant or seedling. Under certain conditions,

however, these sugars are utilized by soil-inhabiting

fungi with the result that the seed or propagative

material rots before it can germinate to produce a

seedling, or else causes the rotting of the young seed-

ling at soil level. An example of such a microorganism

is the saprophytic fungus Pythium ultimum, which

causes the diseases, referred to as pre- and post-

emergence damping-off. Rhizoctonia solani causes

damping-off on a wide range of cultivated plants –

cereals, potato, root and fodder crops, legumes,

and vegetables. On lettuce, this fungus is often asso-

ciated with some Pythium spp. and pathotypes of

Botrytis cinerea. In most cases, the fungus remains

quiescent on the consumable material and only grows

actively when conditions are favorable. Onions are

commonly attacked by Botrytis alli, and beet is often

colonized by Pleospora bjoelingii (Phoma betae in

pycnidial stage).

0005Viruses are no exception in their association with

foods, for several viral ‘mosaics,’‘crinkles,’ and

MICROBIOLOGY/Classification of Microorganisms 3877

‘yellows’ are caused by the virus called arabis mosaic

virus, which mostly affects strawberries, raspberries,

and grapes.

0006 Plant pathologists and agriculturists often refer to

microorganisms as being field or storage microorgan-

isms. Microbial flora of cereals undergo pronounced

and significant changes in the field. Grains may

become colonized by field fungi, and these include

species of Cladosporium, Alternaria, Helminthospor-

ium, and Chaetomium. After harvest, however, the

numbers of these field flora decrease, giving room to

storage fungi, the commonest of which are Penicil-

lium, Aspergillus, and some nonpathogenic species of

Fusarium. When leaves unfold, they act as spore traps

for airborne microbial propagules, some of which

grow and form the phylloplane, or leaf surface flora.

Close observation has revealed that these propagules

can be found on leaves that animals graze and man

uses in cooking or as raw components of salads. The

majority of these are fungi of the Ascomycotina and

the commonest recorded are Cladosporium spp., Epi-

coccum nigrum, Aureobasidium pullulans, and Alter-

nata tenuis. There are frequently true yeasts of the

genera Sporobolomyces and Bullera, the so-called

mirror yeasts on plant leaf surfaces.

0007 An interesting and richer association of yeast in the

wild is to be found with nectaries of flowers and

the surfaces of fruits. The presence of some of these

fungi is a prerequisite in the spontaneous fermenta-

tion of fruit juices, such as grape in the production of

wine. Palm wine obtained from the oil palm (Elaeis

guineensis), date palm (Phoenix dactylifera), and the

raffia palm (Raphia vinifera) in parts of the world are

also fermented in a similar manner by wild epiphytic

and airborne yeasts.

0008 Food crops are commonly colonized by Gram-

negative rods such as Erwinia, Pseudomonas,and

Xanthomonas, but several Gram-positive bacteria

such as Lactobacillus and Leuconostoc are present,

which are important in the production of fermented

vegetable products such as sauerkraut (fermented

pickled cabbage) (Table 1). When leafy vegetables

that are consumed fresh are colonized, it is almost

impossible to eliminate these microflora completely

by ordinary washing, but in most cases they are harm-

less to the consumer.

0009 A rather unusual association of some microorgan-

isms and food plants can be found in the rhizoplane.

Root nodules of the Leguminosae are formed as a

result of a symbiotic association of a bacterium Rhi-

zobium melioloti with root nodules of alfalfa (Medi-

cago sativa). This symbiotic relationship greatly

increases the nitrogen content not only of the soil

but also of the plant crop at maturity. Some mycor-

rhizal associations between fungi and roots of some

food plants not only offer protection to the roots but

also contribute indirectly to their overall crop yield.

Similarly, some microorganisms can establish associ-

ations with members of the botanical family Fabaceae

(Papilionaceae and Leguminosae), which provide

man and other animals with the most important

plant proteins, the pulses. In spite of their low water

content after drying, they are usually attacked by

lipolytic molds of the genera Aspergillus (such as

A. niger, A. tamarii), Penicillium and Paecilomyces.

0010The ability of some soil microorganisms to degrade

complex organic materials makes these microbes

potent spoilage agents, if they are present on foods.

At times, the soil can be a harsh and competitive

environment, and many soil microorganisms adapt

to these sudden changes by producing resistant struc-

tures such as endospores (by the bacterial genera

Bacillus and Clostridium), chlamydospores, and

sclerotia of many fungi (such as Claviceps purpurea

or ergot). The subsequent germination of these struc-

tures is responsible for the occurrence of food spoil-

age and food poisoning caused by the clostridia and

bacilli. The spore-forming anaerobe Clostridium can

be predominantly proteolytic or saccharolytic. Both

of these activities are accompanied by gas production

and cause some infected cans on supermarket shelves

to swell, resulting in the ‘blown can’ effect.

Microorganisms on Food in Transit or in

Storage

0011Food in transit is often damaged by a number of

microorganisms if conditions are ideal for their

growth. Considerable losses of vegetables such as

carrots, potatoes, onions, and celery are caused by

bacteria causing soft rot and the species belonging to

the Genus Erwinia, such as E. carotovora, E. atrosep-

tica (black leg), E. aroideae, and E. chrysnthemi. This

situation is usually worsened when there are bruises

and lesions, but at high temperatures and high humid-

ity, Bacillus polymxya is capable of reducing potato in

storage to a yellow sticky mass with a distinct fruity

odor. Pseudomonas phaseolicola perennates on dwarf

bean (Phaseolus vulgaris), and this same fungus causes

the diseases leaf spot and halo blight.

0012Fungal survival, or their contamination of foods, in

transit is a common phenomenon, and several genera

are involved. Species of the fungus Rhizopus are

capable of causing considerable damage to peaches,

grapes, sweet potato, crucifers, cucurbits, tomatoes

and eggplant (Solanum melongena) and produce soft

rot very rapidly at temperatures above 10



C. Pota-

toes are commonly attacked by Fusarium caeruleum,

causing dry rot of the tuber. Ergot of cereals is a

disease caused by members of the genus Claviceps.

3878 MICROBIOLOGY/Classification of Microorganisms

It is widely distributed throughout the world, and the

most economically important is ergot of rye caused by

Claviceps pupurea. This fungus is important not so

much for the effect it has on the growth of crop but

for the characteristic fungal fruiting structures called

ergot (sclerotia), which can contaminate cereals

during harvest and cause poisoning in man and

animals. Feeding livestock with cleanings from con-

taminated grain or grazing pastures with infected

grass heads can lead to abortions and peripheral

gangrene.

0013Bread can be infected with the bread mold at

several locations, even in the fridge, and it has been

known to cause infections due to colonization by

B. cereus. There have been a number of instances

where survival of pathogens or their toxins have

caused problems in products such as dried herbs,

rice, dried milk, chocolate, pasta, and eggs, and gen-

erally, Salmonella and Staphylococcus aureus have

been associated with these outbreaks. Xerosporic

(nonwater wettable) microorganisms can survive

almost indefinitely on dried products.

tbl0001 Table 1 Foodborne pathogenic bacteria

Organism Food source Illness

Salmonella spp. Poultry, eggs, milk, swine, water,

shrimps, raw meats

Typhoid and typhoid-like fever

Clostridium botulinum Any food with pH above

4.6; all canned meats, honey, vegetables

Foodborne botulism (intoxication)

Staphylococcus aureus Most foods not kept

hot or cold enough

Staphylococcus food poisoning

(staphyloenterotoxicosis)

Yersinia enterolitica Meats, icecreams, milk Yersiniosis, bacteremia, arthritis

Campylobacter jejuni Water, unpasteurized

milk, meat, poultry

Enteritis, gastroenteritis, campylobacteriosis

Listeria monocytogenes Milk, cheese, icecream,

vegetables, fermented raw meats,

all meats raw or smoked

Listeria meningitis

Vibrio cholerae Contaminated water (poor sanitation) Cholera

Vibrio parahaemolyticus Raw improperly cooked or

contaminated fish and shellfish

Gastroenteritis, diarrhea, cramps, nausea

Vibrio vulnificus Oysters, clams, crabs

(raw or contaminated)

Gastroenteritis, wound infection, septicemia

Clostridium perfringens Improperly prepared food: meats,

meat products, gravy

Food poisoning, pig belly disease

Bacillus cereus Meats, milk, vegetables, fish

(vomiting is associated with rice,

potato, pasta, cheese, and

food mixtures)

Diarrhea-type, food poisoning, vomiting

Aeromonas hydrophilia Beef, pork, lamb, poultry,

shellfish, fish

Gastroenteritis to septicemia

Plesiomonas shigelloides Contaminated water or

raw shellfish

Gastroenteritis (self-limiting), fever, chills

Shigella spp, S. sonnei,

S. boydii, S. flexneri, S. dysenteriae

Salads, raw vegetables,

milky dairy products, poultry

Bacillary dysentery

Miscellaneous Gram-negatives:

Klebsiella, Enterobacter, Proteus,

Citrobacter, Aerobacter, Providencia,

and Serratia

Dairy products, raw shellfish,

fresh vegetables, water

Gastroenteritis

Group A Streptococcus spp: S. pyogenes Group A: milk, icecream,

eggs, steamed lobster,

ground ham, potato salad,

egg salad, custard, rice

pudding, shrimp salad

Tonsillitis, high fever, septic sore throat

Group D Streptococcus spp. S. faecalis,

S. faecium, S. durans, S. avium, S. bovis

Dairy products, raw shellfish,

fresh raw vegetables

Scarlet fever, diarrhea, abdominal

cramps, vomiting, septicemia

Enterotoxigenic, Escherichia coli Contaminated water, dairy products,

e.g., semisoft cheeses

Gastroenteritis, travellers’ diarrhea

Enteropathogenic E. coli Raw beef, chicken, and

any food exposed to fecal

contamination

Infantile diarrhea

Enteroinvasive E. coli Hamburger, meat, unpasteurized milk Mild dysentery

MICROBIOLOGY/Classification of Microorganisms 3879

0014 Bananas in transit are subject to several fungal rots,

and the most troublesome and commonest of these,

which is considered largely responsible for the decline

in the quality of Jamaican bananas imported into

England, is attributed to rotting by Gleosporium

musarum. Stone and pome fruits are particularly

prone to brown rot, and the three main fungi involved

belong to the genus Sclerotinia. Sclerotinia fructigena

and Sclerotinia laxa occur in Europe, and Sclerotinia

fructicola occurs in the USA. Apples infected by Scler-

otinia fructigena are initially covered with conidial

cushions, and the infected fruits gradually shrivel and

become mummified. A species of this fungus Sclero-

tinia sclerotiorum is particularly dangerous, because

it can continue to cause rotting of vegetables at

temperatures near freezing point. Fungi also cause

considerable damage to citrus fruits in transit: Peni-

cillium italicum and Penicillium digitatum cause the

diseases called blue and green mold, respectively, and

Penicillium expansum causes a soft rot in apples.

Other common diseases of apples and pears include

the black spot or scab caused by the Ascomycotina

fungus called Venturia inaequalis (anamorph

Spilocaea pomi ¼Fusicladium dendriticum). Lemons

are transported under relatively high temperatures,

and this condition permits the development of

Phytophthora brown rot.

0015 An especially widespread mold on fruit and vege-

tables is the gray mold Botrytis cinerea, which is an

imperfect stage of the Ascomycete, Botryotinia fuck-

eliana ( ¼Sclerotinia fuckeliana). In canned fruits, the

low pH and heat treatment means that most molds

are killed, but some members of the Eurotiales are

sufficiently heat-resistant and survive. The best

known are species of Byssochlamys, but recent spoil-

age of some exotic fruits in canneries has been due to

Neosartorya fischeri (anamorph Aspergillus fischer-

ianus) and Talaromyces flavus var. macrosporus

(anamorph Penicillium sp.).

0016 Survival of remnants of fungal pathogens on seeds is

very common: it is usual to find a reservoir of the loose

smut disease agent of wheat and barley Ustilago nuda in

the scutellum. Similarly, the hyphae of the fungus that

causes loose smut of oats, Ustilago avenae,arecommon

on the embryo, seed, or fruit coat of oats, and Tilletia

caries and Septoria apiicola can be commonly detected

on the seeds of wheat and celery, respectively. Species

of the fungus Aspergillus can cause considerable deteri-

oration of stored grain. The best studied is A. flavus,

which is also capable of producing several toxic mater-

ials, collectively known as aflatoxin. This toxin, which is

carcinogenic, has been found in most stored products

such as peanuts, dates, and an array of foods.

0017 Relatively few viruses survive on, and are transmit-

ted by, seeds, and lettuce mosaic virus is a common

example. When crops are harvested, they may harbor

several microbes. As a rule, field microbes give way to

the colonization of storage microorganisms, often

resulting in fruit and fleshy storage organs rotting,

and dry cereal grains becoming moldy. The pathogens

responsible for this type of spoilage are frequently

those that do not develop at all, or develop only to a

limited extent on the host in the field. An example of

such an organism is Fusarium solani var. coeruleum,

which causes dry rot of potato tubers. Similarly,

potato blight (Phytophthora infestans) can be initi-

ated from tubers. The air of farmyard barns may

contain many millions of spores of Actinomycetes

per cubic meter. Spores of some species such as

Thermoactinomyces vulgaris and Micropolyspora

faeni cause lung allergy in farmers, and some geos-

min-producing strains of Streptomyces may be re-

sponsible for earthy odors and off-flavors in potable

water; also, geosmin can impart earthy taints to food

such as shellfish.

Microorganisms in Water

0018Aquatic environments represent the largest part of the

biosphere, and many species of microorganisms are

found in both marine and freshwater environments.

Open oceans contain salt and many marine bacteria,

referred to as oligotrophic psychrophiles, which have

a requirement for salt and can grow at relatively low

temperatures. The surfaces of fish caught from cold

water in the open sea contain psychrophilic and psy-

chrotrophic bacterial flora that are capable of break-

ing down proteins, polysaccharides, and lipids, and

can double in numbers at refrigeration temperatures

of 0–7



C in as short a time as 10 h. The implication of

this is that a single bacterium on freshly caught fish

can multiply to 2

or between 10

and 10

in just 9

days, and in this situation, cold-stored fresh fish starts

giving off off-odors.

0019The sea has been used by man as a dumping ground

for sewage and other waste products. Unfortunately,

many shellfish used for food grow in these polluted

coastal waters and actually feed by filtering out par-

ticles from large volumes of seawater. Therefore,

there is always a high risk of contamination by enteric

organisms from infected individuals, and the mi-

crobes concentrate in numbers within the organism

as a result of the filter-feeding habits of shellfish.

Severe diseases such as hepatitis and typhoid fever,

and milder illnesses such as gastroenteritis, have been

caused by eating contaminated oysters and mussels

that look sound in appearance and taste normal. In

warmer seas with unpolluted water, high numbers of

the bacterium Vibrio parahaemolyticus may also be

concentrated through the filter feeding of shellfish.

3880 MICROBIOLOGY/Classification of Microorganisms

This bacterium then becomes part of the stable com-

mensal enteric flora and has been responsible for

episodes of food poisoning associated with seafood.

0020 Fresh water from lakes and rivers has a complex

flora, which includes genuinely aquatic microbial

species as well as those introduced from terrestrial,

animal, and plant sources. Like other water sources,

fresh water may act as a repository and vehicle for

bacteria, protozoa, and viruses of fecal origin, which

can also cause diseases.

0021 Fungi are also found in marine and fresh waters,

but they are not as important in their association

with food as the groups of microorganisms describ-

ed above. There are true aquatic fungi, and these

include some that are pathogens of molluscs and

fish. The most well-adapted aquatic fungi belong to

all the major groups of terrestrial fungi, namely: Asco-

mycotina, Basidiomycotina, Deuteromycotina, and

Zygomycotina. There is the possibility that some of

these could be responsible for spoilage of some food

commodities, including salad crops cultivated with

overhead irrigation from rivers or lakes. The aquatic

photosynthetic microorganisms, the cyanobacteria

(or blue–green algae), and the eukaryotic dinoflagel-

lates are groups of microorganisms that may also

become concentrated in shellfish and can cause severe

illness such as paralytic shellfish poisoning.

0022 A significant global problem is the viral contamina-

tion of water. In the past, about half of the foodborne

disease outbreaks through water were unrecogniz-

ed, primarily as a result of inadequate diagnostic

methods and sampling. Recently, with improved

diagnostic methods, it has been established that

most of these food and waterborne outbreaks are

caused by caliciviruses and are a major cause of sea-

food associated gastroenteritis.

0023 Bacterial strains of the genus Aeromonas are well-

recognized enteropathogens of man. The main source

of infection by this organism seems to be untreated

water, because these microorganisms can be found

in virtually all aquatic environments. Furthermore,

some enterotoxigenic pathotypes of Aeromonas are

capable of rapid growth and toxin production at

temperatures as low as 5



C. This means that vege-

table products irrigated with contaminated water

may reach critical Aeromonas levels during refriger-

ation and could represent a serious public health

hazard when these vegetables are consumed as

uncooked salads.

Microorganisms in Milk

0024 Raw milk becomes laden with microorganisms from

three sources: udder interior, teat exterior and its

surrounding, and the milking and milk handling

equipment. Milk expressed aseptically from a healthy

cow may be sterile or contain low numbers of micro-

organisms, usually about 10

–10

cfu ml

1

. The most

frequently isolated organisms are micrococci, strepto-

cocci, and Corynebacterium bovis. Higher microbial

counts are often seen if the animals suffer from

mastitis, and under these circumstances, many types

of bacteria are seen. The most important of

these are the potential human pathogens Staphylo-

coccus aureus, Escherichia coli, Streptococcus

agalactiae, Streptococcus uberis, Pseudomonas aeru-

ginosa, and Corynebacterium pyogenes. Occasionally

other human pathogens, such as Salmonella, Listeria

monocytogenes, Mycobacterium bovis,andMyco-

bacterium tuberculosis, are isolated.

0025The udder exterior, the teats, and the cow’s imme-

diate environment such as bedding and manure

can also be a source of heavy contamination

(10

cfu ml

1

) of the milk. In these situations, the

microorganisms involved are mostly human patho-

gens such as E. coli, Helicobacter (Campylobacter)

from bedding and manure, Salmonella and Bacillus

spp. from soil, and Clostridium butyricum and Clos-

tridium tyrobutyricum from silage. These Clostri-

dium spp. are the cause of a form of spoilage called

‘late blowing cheese.’ In some parts of the world, a

potent contaminant of milk and meats is caused by

Brucella spp.

0026In most developed countries, milk is chilled soon

after it is issued from the cow, and under these cir-

cumstances, only psychrotrophic organisms are found

in raw milk. The most common are Gram-negative

rods of the genera Pseudomonas, Acinetobacter, Alca-

ligenes,andFlavobacterium, the psychrotrophic coli-

form Aerobacter, and Gram-positive Bacillus spp. In

order to reduce the numbers of harmful organisms,

milk is either pasteurized or ultraheat-treated. Raw

milk after pasteurization may contain organisms,

referred to as thermodurics, that can survive this pro-

cess. These organisms are generally Gram-positive,

such as the spore-forming bacteria and members of

the genera Microbacterium, Micrococcus, Enterococ-

cus,andLactobacillus, but it is usual to find some

strains of the Gram-negative bacterium Alcaligenes

tolerans. Spoilage of pasteurized milk is due to the

growth in milk of the Gram-negative rods Pseudomo-

nas, Alcaligenes, Acinetobacter and Psychrobacter,

which may be inadvertently introduced after pasteur-

ization. Salmonella has been isolated from icecream

that has been stored at 23



C for 7 years.

Microorganisms on Meat

0027In theory, freshly harvested meat should be relatively

free from microorganisms, but microbial numbers

MICROBIOLOGY/Classification of Microorganisms 3881

detected in aseptically sampled tissues contain some

microbes, usually less than 10 cfu kg

1

. There is evi-

dence, however, that these numbers can increase

under conditions of stress and if the animal is

suffering from an infection, as in the case in Bru-

cella-infected animals. Most meat contamination is

from the heavily colonized areas of the animal, such

as the skin (fleece) and the gastrointestinal tract, and

the type and numbers found will reflect both the

animal’s indigenous microflora and its environment.

The animal hide carries mixed microbial population

of micrococci, staphylococci, pseudomonads, yeasts,

and molds as well as organisms derived from soil and

feces. After dressing and chilling, the surface micro-

bial numbers are typically of the order of 10

–10

cfu

2

and are usually higher in sheep carcasses than in

beef, and even higher still in pigs. In some parts of the

world, the fur on sheep, cattle and pigs is thoroughly

burned soon after slaughtering the animal. Tradition-

ally, the method is used as a way of imparting flavor

to the meat, but it should also be lauded and seen as a

first step in reducing the microbial numbers on the

skin that could otherwise contaminate the flesh. Like-

wise, after defeathering, in some traditions, birds are

flamed before the flesh is cut, and this treatment also

greatly reduces the potential contamination of the

poultry meat by microbes on the skin.

0028 Species of the genus Brucella are known human

pathogens that can cause undulant fever, and are asso-

ciated with a particular animal host: B. abortus in

cattle, B. melitensis in sheep and goats, B. suis in pigs,

and B. canis in dogs. Even though the diseases are

contracted from close contact with infected animals,

they can also be contracted by the consumption of

milk, milk products, and meat from these animals.

0029 The processing of poultry is different from red

meat, and this has microbiological implications: an

active processing plant that can handle 12 000 birds

per hour leaves little chance for effective sanitation

and favors the spread of microbes between carcasses.

After scalding, birds are mechanically defeathered,

and a number of studies have suggested that this

method actively passes organisms like Salmonella

from one carcass to the other. The intestinal tract of

poultry also contains high numbers of the human

pathogens Salmonella and Helicobacter (Campylo-

bacter); these are easily passed on and are the two

major causes of foodborne illness in the UK. Interest-

ingly, Campylobacter coli and C. jejuni do not grow

at temperatures below 30



C and only become patho-

genic when food contaminated by these bacteria is

consumed and the microbes start thriving under the

higher human body temperature. Being microaero-

phillic, they are also able to survive the low-oxygen

conditions of modern storage processes.

0030The first indication of spoilage of meat is the pro-

duction of off-odors, which become apparent when

the microbial numbers in meat reach 10

cfu cm

2

Aerobic storage of chilled red meats, whether covered

or uncovered, produces a high redox potential at the

meat surface that favors the growth of psychrotrophic

aerobes. Nonfermentative Gram-negative rods grow

most rapidly, causing spoilage, and the principal

genera are Pseudomonas, Acinetobacter, Psychrobac-

ter, Pseudomonas fragi, and Pseudomonas lundensis.

Other microbes that form a minor component of

the spoilage microflora are members of the Entero-

bacteriaceae, such as Serratia liquefasciens and

Enterobacter agglomerans, lactic acid bacteria and

the Gram-positive bacterium Brochothrix thermo-

sphacta.

0031In vacuum-packed meat, the microflora of the

meat changes as a result of the accumulation of

and lack of oxygen. This restricts the growth

of Pseudomonas, and colonization is dominated by

Gram-positives, lactic acid bacteria of the genera

Lactobacillus, Carnobacterium, and Leuconostoc.

0032The perception of spoilage is subject to a number of

influences, particularly social: foods acceptable in

some cultures are unacceptable in others. Matured

cheeses and game birds (e.g., pheasants) that have

been hung for several weeks are seen in some cultures

as objectionable, but these same products are treas-

ured and sold for large amounts of money to the

affluent in other societies.

Microorganisms on Fish (Teleosts and

Elasmobranchs), Crustaceans, and

Molluscs

0033Like meat, the muscle and internal organs of freshly

caught healthy fish are usually sterile, but the skin,

gills, and alimentary track carry large numbers of

bacteria. These can be as high as 10

on the skin

and up to 10

in the gills and the gut, and these are

mainly Gram-negatives of the genera Pseudomonas,

Shewanella, Psychrobacter, Vibrio, Flavobacterium,

and Cytophaga, as well as a few Gram-positive

micrococci and coryneforms.

0034Fish can be easily contaminated by human patho-

gens during handling on board, at the dock, and at

markets when they are being offered for sale. The

common foodborne illness pathogens associated

with fish are Vibrio cholerae, Vibrio parahaemolyti-

cus, Vibrio vulnificus, Clostridium botulinum Type E,

enteric viruses, and those that cause Scombroid fish

poisoning and paralytic shellfish poisoning.

0035Spoilage of chilled fish is mainly due to the activity

of the psychrotrophic Gram-negative rods Shewa-

nella putrefaciens and some Pseudomonas species.

3882 MICROBIOLOGY/Classification of Microorganisms

Shewanella putrefaciens can grow under a variety of

conditions, producing trimethylamine and hydrogen

sulfide to spoil even vacuum-packed fish. Work in

Denmark has demonstrated that marine Vibrios like

Photobacterium phosphorous cause nonsulfurous

spoilage of fish produce.

Foodborne Viruses

0036 Viruses are obligate intracellular parasites and can

only multiply in a susceptible host cell. Recently,

viruses have been recognized as an important source

of foodborne diseases (Table 2), and over one hun-

dred human enteric viruses have been implicated.

These viruses are spread mainly by the fecal–oral

route, making foods for human consumption a poten-

tial route for transmission. However, the genus en-

terovirus includes the polio and the hepatitis A and E

viruses, all of which are known to be foodborne.

Hepatitis A is transmitted by the fecal–oral route,

primarily spreads by person-to-person contact, but

food- and waterborne outbreaks do occur. Foods

such as milk, strawberries, raspberries, lettuce, and

shellfish are common food vehicles.

0037 The causative agent of enterically transmitted

nonA nonB virus, which is now designated as hepa-

titis E virus, is also transmitted fecal–orally. Other

viruses have been implicated in gastroenteritis by

their sheer large numbers (10

–10

) and are also

known to cause diarrhea and other foodborne gastro-

enteritis. Most of these enteric viruses may be intro-

duced into foods either as primary contamination at

source of food production (harvest) or as secondary

contamination during handling, preparation, or serv-

ing. Fruits and vegetables that are fertilized with

human excrement are thought to be the sole source

of contamination. Shellfish are grown commonly in

shallow, inshore, coastal waters and are often con-

taminated with viruses. The problem is compounded

by the fact that some shellfish such as oysters

are consumed with little or no cooking (as in most

Mediterranean countries). In the UK, strict guidelines

aimed at inactivating the hepatitis A virus exist for the

cooking of cockles.

0038Spongiform encephalopathies (SEs), Creutzfeldt–

Jakob disease, and other scrapies are degenerative

disorders of the brain caused by the so-called ‘slow

viruses,’ which are contracted by consumption of

meat from infected animals. Lassa fever, which occurs

in Nigeria, Guinea, Liberia, and Sierra Leone, is

caused by an arenavirus in infected rats, the main

reservoir of infection.

Foodborne Protozoa

0039Only a few protozoa are associated with food or are

foodborne (Table 3); the flagellate Giardia, the

amoeboid Entamoeba and three sporozoids of the

phylum Apicomplexa, which include the genera Tox-

oplasma, Sarcocystis,andCryptosporidium, are some

of the commonly encountered protozoa.

0040Giardia lamblia (also called G. intestinalis or Lam-

blia intestinalis) survives on food and water as cysts.

The cysts, which are aided by gastric juices to release

the infective flagellate protozoa, have been found on

salad vegetables such as lettuce, fruits such as straw-

berries, and any food that is washed with contamin-

ated water or handled by infected persons. The cysts

are resistant to chlorination but can be disabled if the

food is well cooked. Entamoeba histolytica, which

causes amoeboid dysentery, is widespread and almost

endemic in many poor communities. It is estimated

that an actively infected person can shed up to 50

million cysts per day, and the potential of these to

cause fecal–oral infections cannot be overemphasized.

It has been suggested from epidemiological studies

that foods such as raw sausage are a risk factor in the

sporozoid infection cryptosporidiosis. The organism

Cryptosporidium parvum can go through its entire

life cycle in a single host, and the host could be

human, cattle, or sheep. Two species of Sarcocystis,

however, are obligate parasites: S. hominis, which

tbl0002 Table 2 Foodborne pathogenic viruses

Organism Food source Illness

Hepatitis A Contaminated water and food,

sandwiches, fruit and fruit juices,

milk and milk products,

vegetables, salads, shellfish

and iced drinks

Mild fever, malaise, nausea, anorexia,

abdominal discomfort and jaundice

Hepatitis E Water Malaise, anorexia, abdominal pain, arthralgia, fever

Rotavirus Salads, fruits, hors d’ouvres Viral gastroenteritis, infantile diarrhea, winter diarrhea

Norwalk viruses Water and foods Nausea, vomiting, diarrhea, abdominal pain

Other gastroenteritis viruses Food and water Nonbacterial viral gastroenteritis

Parvo-like virus Shellfish Viral gastroenteritis

MICROBIOLOGY/Classification of Microorganisms 3883