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

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defects are revolting to the consumer and make it

unacceptable for consumption. Food is also con-

sidered spoiled if the potential for the spread of food-

borne disease exists. For example, food contaminated

with high numbers of Staphylococcus aureus and

possibly staphylococcal enterotoxin would not have

any obvious defects that would make it apparently

unacceptable, but it could make the consumer very

ill and from this point of view it is spoiled. Food

contaminated with industrial chemicals, pesticides,

herbicides, or any material that should not be in the

food would be considered spoiled. There are many

facets of food spoilage. In this article, food spoilage

caused by bacteria is reviewed. Foodborne illness is

discussed in other sections of the Encyclopedia.(See

Wastage of Food.)

Food as a Habitat for Bacteria

0002 In its natural state, food, whether derived from

animals or plants, is very susceptible to the action of

bacteria and is easily spoiled by their metabolic activ-

ities. The processing of food is designed, among other

things, to control the activity of bacteria and other

microbes to preserve the food for later use. As food is

processed, the type of bacterial spoilage that may

occur will change. The major thrust of this article

will be to describe how varying process methods

affect food spoilage by bacteria. The growth of bac-

teria in foods is affected by several factors inherent in

the food or by conditions external to the food. These

include the acidity or pH of the food, the availability

of water (water activity, a

), the oxidation reduction

potential (redox or E

) of the food and the environ-

ment, availability of the nutrients in the food, the

temperature of the food and the environment, and

time available for bacterial growth to occur. (See pH

– Principles and Measurement; Water Activity: Effect

on Food Stability.)

Processing of Food and Bacterial Spoilage

0003 The extent of processing of foods varies. Some foods

are not processed prior to use and are very perishable.

Others are lightly processed and are easily spoiled

by bacterial action. The use of two or more preserva-

tion methods will give a food product additional

stability, but does not make it immune to bacterial

spoilage. This process of using one or more minimal

preservation processes on a food to extend its quality

retention time is referred to as the ‘hurdles concept.’

By adding another process to the food a hurdle is

created, that is, one more factor that the bacteria

have to overcome before they will grow and spoil

the food. Thus the use of several hurdles should

have a very positive effect on the quality retention

time. There are a significant number of high-quality

minimally processed foods that utilize the hurdles

concept to control bacterial spoilage and effectively

increase quality retention.

0004Foods given a more severe preservation process,

such as drying or canning (high-temperature thermal

process), are not as easily spoiled by bacterial action.

With these concepts in mind it is possible to classify

foods into spoilage potential categories based on the

type of preservation process applied to it:

0005Highly perishable, no preservation process (such

as fresh poultry) with a quality retention time of

1–3 days

0006Semiperishable, lightly processed (such as pasteur-

ized milk) with a refrigerated quality retention

time of 1–3 weeks

0007Semishelf-stable, two or more preservation pro-

cesses used (the hurdles concept), such as vacuum-

packaged cooked meat products, with a quality

retention time from 1 to 4 months

0008Shelf-stable, highly processed foods, such as

canned vegetables or dried milk products with a

quality retention time exceeding 1 year

0009Thus, the processing or lack of processing that the

food receives significantly influences the type of bac-

terial spoilage that occurs in foods. By developing and

understanding the factors affecting the growth of

bacteria, such as the chemical, physical, and compos-

itional properties of food and the processing applied

to the food, it is possible to predict with some re-

liability the type of bacterial spoilage that may occur

in food. (See Canning: Principles; Drying: Theory of

Air-drying.)

The Spoilage of Food by Bacteria

0010Bacterial spoilage of food occurs when a number of

factors are in place:

0011The food must be contaminated with spoilage

bacteria

0012The food must be suitable for growth of the con-

taminating bacteria

0013The environment associated with the food must

support microbial growth

0014The bacteria must grow and produce metabolites

which ‘spoil’ the food

0015There must be sufficient time for the bacteria to

grow

0016Control of these five factors will markedly influ-

ence the growth of bacteria in food and the resultant

spoilage.

SPOILAGE/Bacterial Spoilage 5507

Source of Bacteria in Food

0017 Bacteria come into contact with or contaminate food

from several sources. Food obtained from plants that

is consumed by humans is in direct contact with soil.

Fertile soil will contain up to 10

microbes per gram

of soil. Consequently, foods that grow in or on the

soil will be contaminated with significant numbers of

bacteria. Animals used as food for humans are

contaminated on the outside by soil and manure bac-

teria and internally by bacteria associated with the

digestive system of the animal. When slaughtered, the

flesh becomes contaminated with the internal bac-

teria as well as the external ones. Foods obtained

from marine sources are contaminated by bacteria

from the water in which they live and by bacteria in

their digestive system.

0018 Animal, plant and marine foods have native or

indigenous microflora associated with them. In gen-

eral, bacteria on the exterior of these foods are usu-

ally aerobic and frequently psychrotrophic, whereas,

bacteria in the interior of the animal, plant, or marine

food will be obligate or facultative anaerobes. The

interior of these food sources will have reduced E

values or a negative oxidation reduction potential,

creating anaerobic conditions, which encourages the

development of these organisms. Regardless of the

source of the organisms, under the right conditions

all are capable of causing food spoilage.

0019 Food is also contaminated with bacteria from

people who handle the food. These bacteria are usu-

ally mesophilic and may occasionally be pathogenic.

A primary source of contamination of food with

spoilage bacteria is the equipment used to handle

and process the food. If the equipment is not clean,

microcolonies, called biofilms, composed of surface

dirt and bacteria will develop and consequently mil-

lions of bacteria will be present on the surface: when

the food comes in contact with the biofilms on the

surface they can be transferred to the food. This

concept of bacteria transfer to foods from biofilms

is referred to as the biotransfer potential. Control of

direct human contact with the food and proper

cleaning and sanitizing of food contact surfaces and

nonfood contact surfaces are critical in preventing

bacterial contamination of foods. (See Cleaning Pro-

cedures in the Factory: Overall Approach.)

Bacterial Food Spoilage Based on

Preservation Processes

Highly Perishable Foods

0020 Highly perishable foods are those that have been

harvested or slaughtered and are utilized with little

or no further processing to prevent bacterial spoilage.

This category includes, but is not limited to, the

following fresh foods: raw vegetables, raw fruits,

raw milk, fish, poultry, and red meats. Of these food

groups, fresh raw fruits are the least susceptible to

bacterial spoilage since the pH of the fruits retards

bacterial growth. The environment in which the food

is maintained affects bacterial spoilage of these foods.

Under low-temperature storage, between 0



C and



C, the primary bacterial spoilage is caused by

psychrotrophic bacteria. These organisms are able

to grow slowly at low temperatures; they have opti-

mum growth temperatures in the mesophilic range

and could also cause spoilage of these foods at higher

temperatures. The majority of these bacteria are in

the family Pseudomonaceae and are species in the

genera Pseudomonas, Xanthomonas, Gluconobac-

teria, Achromobacter, Flavorbacterium,andAlcali-

genes. Growth of these bacteria in highly perishable

foods results in a variety of sensory defects (off-

flavors – putrid, rancid, bitter, etc. – formation of

slime, color changes, or strong odors).

0021The temperature of raw unprocessed foods, in es-

sence, selects the type of bacteria that will grow and

spoil the food. If these foods are stored at ambient

temperatures of 18–43



C, mesophilic bacteria of

many types will grow and spoil the food. Species in

the genera Clostridium, Bacillus, Erwina, Streptococ-

cus, Lactobacillus, Escherichia, Proteus, Enterobac-

ter, and many others, will grow and cause spoilage of

the food.

0022It should be clear from the discussion up to this

point that many different types of bacteria are able to

grow on raw, unprocessed foods. Even refrigeration

will not stop bacterial spoilage of these foods. The

identification of genus and species of the bacteria

causing food spoilage is not critical to preventing

food spoilage; however, it may be useful to identify

the bacteria if the source of the spoilage organisms is

important. What is critical is that bacterial spoilage of

food is recognized and that appropriate steps are

taken to control or prevent the spoilage. (See Con-

trolled-atmosphere Storage: Applications for Bulk

Storage of Foodstuffs; Fish: Spoilage of Seafood;

Meat: Preservation.)

0023Food is processed to prevent spoilage. As the inten-

sity of the preservation process increases, the types of

bacterial spoilage are changed or eliminated. Spoilage

of the other three categories of processed foods

reflects these changes.

Semiperishable or Lightly Processed Foods

0024Semiperishable or lightly processed foods are subject

to much the same type of spoilage as the unprocessed

or perishable food described above. The preservation

5508 SPOILAGE/Bacterial Spoilage

processes used with this type of food are usually a

mild heat treatment coupled with refrigerated stor-

age, below 7



C. Pasteurized refrigerated dairy prod-

ucts or pasteurized refrigerated egg products are good

examples of lightly processed foods. The heat treat-

ment used with these foods will usually destroy

psychrotrophic bacteria and nonspore-forming meso-

philic bacteria, but the handling of the foods after

heat processing usually results in contamination of

these products with spoilage-type bacteria. Such

spoilage bacteria have been found in unclean equip-

ment, moisture droplets on the equipment, and in

liquid drain traps. During subsequent refrigerated

storage, the psychrotrophic bacteria will grow and,

if storage time is long enough, spoilage will result.

The same genera given above for the raw or unpro-

cessed foods can be involved in the spoilage of the

lightly processed foods. Foods that have received this

type of processing will usually maintain desired qual-

ity attributes for 1–3 weeks. (See Heat Treatment:

Chemical and Microbiological Changes; Pasteuriza-

tion: Principles.)

Semishelf-stable Foods

0025 Semishelf-stable foods are preserved utilizing more

than one preservation process. This process has been

referred to as the hurdles concept. The hypothesis of

the hurdles concept is that each less than lethal pre-

servation process becomes one more hurdle for the

bacteria to overcome before they can initiate growth

in the food. These types of foods are becoming popu-

lar as they best reflect the quality attributes of fresh

foods. They are often referred to as ‘fresh-like’ or

‘chef-like,’ implying a freshly prepared product,

which they are not. Foods that have been processed

using the hurdles concept will usually maintain

desired quality attributes for anywhere from 1 to 6

months.

0026 This concept might best be explained by following a

product through such a series of processes or hurdles.

For example, in the processing of cooked beef prod-

ucts, such as roast beef, several steps are involved.

Usually the processor will receive ‘box beef’ which

would be containers of the particular cut of meat to

be used. These cuts were initially processed in another

facility and shipped by refrigerated transport. The first

step in the processing of the beef roasts involves trim-

ming and shaping the meat piece. This removes some

surface contamination but does little to extend the

shelf-life. The second step might involve massaging

the meat and adding salt and other seasonings. The

salt and seasoning will have minimal effect on exten-

sion of shelf-life, unless the salt concentration is above

4 or 5%. If sodium nitrite is used in the seasonings,

some inhibition of spore germination may result. This

would be the first hurdle.

0027The seasoned, massaged meat is next put into

heavy polyethylene cook bags and slowly cooked in

water to the desired internal temperature. This pro-

cess usually takes several hours and should result in

the destruction of psychrotrophic and mesophilic

spoilage bacteria, the most common types of bacteria

that might spoil this product. The cooking process is a

major hurdle as it effectively destroys most spoilage

organisms.

0028The cooked meat is cooled to less than 7



C and the

cook bag removed. It is at this point in the process

that recontamination with psychrotrophic and

mesophilic spoilage bacteria can occur. The meat is

cut into pieces of a size suitable for resale, rebagged in

oxygen impermeable polyethylene bags and vacuum-

sealed. The vacuum package changes the oxidation

reduction potential in the package and prevents the

growth of aerobic psychrotrophic bacteria. The fin-

ished package should be maintained at low tempera-

ture – less than 2



C – until utilized.

0029A cooked beef product, processed as described,

should have a shelf-life of at least 60 days, if not

120 days. It is not shelf-stable, as spoilage will occur

– usually, thermoduric, psychrotrophic, facultative;

heterofermentative lactobacilli will cause spoilage

which becomes apparent by the swelling of the bag

caused by the gas produced and acid flavor of the

product.

0030A further look at each step will help to form an

understanding of how the hurdle process achieves

better maintenance of quality attributes in the food.

(See Preservation of Food; Chilled Storage: Packaging

Under Vacuum.)

0031The cooking step will kill the potential psychro-

trophic spoilage bacteria, but others, such as thermo-

duric bacteria and spore-forming bacteria, will

survive the heat process. The addition of salt and

nitrite to the meat will deter the growth of spore-

forming bacteria, but will have little effect on non-

spore-forming bacteria. Vacuum packaging changes

the E

from positive to negative, which inhibits the

outgrowth of psychrotrophic aerobic spoilers but

allows the growth of anaerobic and facultative anaer-

obic bacteria. The endresult is that the meat will

eventually spoil. In other words, it becomes esthetic-

ally unacceptable as a result of the growth of thermo-

duric, psychrotrophic, facultative anaerobic bacteria

that grow slowly at refrigeration temperatures.

Shelf-stable Foods

0032Shelf-stable foods have undergone preservation pro-

cesses that have produced foods that are considered

SPOILAGE/Bacterial Spoilage 5509

to be ‘commercially sterile,’ i.e., will not spoil or

cause disease under normal conditions of handling

and distribution. These foods are not completely ster-

ile and are subject to some type of bacterial spoilage.

For example, aciduric and thermoduric bacteria may

spoil foods rendered shelf-stable by reduction of the

pH to less than 4.6 and application of a pasteuriza-

tion heat treatment. Certain species of Lactobacillus,

Clostridium,andBacillus are capable of surviving a

pasteurization heat process and, under the right con-

ditions, will grow in high-acid foods. It is generally

recognized that high-acid foods are more susceptible

to spoilage by yeasts and molds but, as indicated

above, some bacteria will grow and spoil even heat-

processed acid foods.

0033 Canned foods are given a severe heat process,

which is primarily designed to destroy spores of Clos-

tridium botulinum. Other spore-forming bacteria

such as C. sporogenes PA 3679 and Bacillus stearo-

thermophilus will not be destroyed by a thermal pro-

cess designed to control C. botulinum and

subsequently may grow in canned foods. Canned

food spoilage, referred to as ‘flat-sour’ spoilage, is

caused by the outgrowth of B. stearothermophilus,

which produces acid but no gas in the canned food.

Other Bacillus may also survive minimal heat process

and cause spoilage of canned foods.

0034 The outgrowth of spores of C. sporogenes in

canned foods produces considerable amounts of nox-

ious gas and may lead to rupture of the cans. Canned

food spoilage will also occur if the food has been

underprocessed, i.e., not given sufficient heat treat-

ment to produce a commercially sterile product.

Spore-forming bacteria which have survived the pro-

cess usually cause canned food spoilage of this type.

This type of spoilage is apparent from the sour or

putrid odor and frothy or viscous appearance of the

spoiled canned food. (See Canning: Quality Changes

During Canning.)

0035 Failure of the double seam in canned foods results

in what is termed ‘leaker spoilage.’ This type of

spoilage is characterized by the presence of several

different types of bacteria in the food. These bacteria

may cross the defective double seam from the

cooling water, dirty conveyor system, can unscram-

blers, or other can-handling equipment. Foods ther-

mally processed in glass containers will spoil in

much the same manner if the closure mechanism

used on the glass jar is defective or does not seal

properly.

0036 Dried foods are also considered to be shelf-stable

or ‘commercially sterile.’ The available water in dry

food systems is less than 0.80 and, as a result, they are

not subject to spoilage by bacteria as long as the

available water remains low. Yeasts and molds are

more tolerant to low available water and may spoil

these type of foods if the a

is more than 0.60 but less

than 0.80. Foods preserved by controlling water

activity are more frequently ‘spoiled’ by the action

of enzymes than by direct bacterial growth in the

foods. (See Drying: Theory of Air-drying.)

0037The spoilage of food by bacteria is preventable if the

food is processed and handled properly. The preserva-

tion processes used affect the probability and type of

spoilage that will occur. The greater the number of

hurdles that the bacteria have to overcome to grow,

the longer the time for spoilage to occur. Contamin-

ation with spoilage bacteria can occur at any point in

the system that transfers food from the point of initial

production to final consumption. Constant attention

to the prevention of bacterial contamination of food

at each of these process steps will insure a continued

safe and wholesome food supply.

See also: Canning: Principles; Quality Changes During

Canning; Chilled Storage: Packaging Under Vacuum;

Cleaning Procedures in the Factory: Overall Approach;

Contamination of Food; Controlled-atmosphere

Storage: Applications for Bulk Storage of Foodstuffs;

Drying: Theory of Air-drying; Fish: Spoilage of Seafood;

Heat Treatment: Chemical and Microbiological Changes;

Meat: Preservation; Pasteurization: Principles; pH –

Principles and Measurement; Preservation of Food;

Wastage of Food; Water Activity: Effect on Food

Stability

Further Reading

Hood SK and Zottola EA (1995) Biofilms in food process-

ing. Food Control 6: 9–18.

Jay JJ (1996) Modern Food Microbiology, 5th edn. New

York: Chapman and Hall.

Potter NH and Hotchkiss JH (1995) Food Science, 5th edn.

New York: Chapman and Hall.

Ray B (1996) Fundamental Food Microbiology. CRC Press

Zottola EA (1994) Microbes, hurdles, food safety and pro-

cess optimization. In: Singh RP and Olivereira FAR (eds)

Minimal Processing of Foods and Process Optimization:

An Interface. Boca Raton: CRC Press.

Zottola EA and Sasahara KC (1994) Microbial biofilms in

the food processing industry – should they be a concern?

International Journal of Food Microbiology 23:

125–148.

Zottola EA and Smith LB (1990) Pathogenic bacteria

in meat and meat products. In: Pearson AM and

Dutson TR (eds) Meat and Health Advances in

Meat Research, vol. 6. London: Elsevier Science

Publishers.

5510 SPOILAGE/Bacterial Spoilage

Fungi in Food – An Overview

L B Bullerman, University of Nebraska-Lincoln,

Lincoln, NE, USA

Introduction

0001 The kingdom Fungi includes eukaryotic organisms

which range from microscopic, unicellular yeasts, to

multicellular molds, to the macroscopic mushrooms.

Fungi are heterotrophic organisms which obtain food

by absorption and require organic compounds for

energy and carbon. In terms of food safety and food

spoilage by fungi, we are concerned primarily with

molds (microfungi) and yeasts. (See Mushrooms and

Truffles: Classification and Morphology.)

Molds

0002 Molds are eukaryotic, multicellular, multinucleate,

filamentous organisms that grow as compact masses

of intertwining, branching, hairlike filaments. The

total mold organism can frequently grow to macro-

scopic size and be visible to the unaided eye. Thus, the

molds are not true microorganisms, but parts of mold

structures are microscopic in size. Molds are some-

times referred to as microfungi because they are much

smaller than the so-called macrofungi, such as mush-

rooms. The individual mold filaments are called

hyphae (singular: hypha) and a mass of these branch-

ing filaments, forming a mold colony or portion of

mold growth, is referred to as a mycelium or (plural)

mycelia. The hyphae may be submerged, or growing

in a food substrate. The submerged hyphae, also

called vegetative hyphae, serve to anchor the mold

to the substrate and take up nutrients and water by

absorption. In this respect they are not unlike plant

roots. Hyphae that grow above the substrate, the

visible part of the mold, are called aerial or fertile

hyphae. They are called fertile because they give rise

to reproductive structures known as conidiophores

or sporangiophores which produce millions of spores

– conidiospores, or conidia, and sporangiospores, or

sporangia.

0003 Conidiospores are produced free by special cells on

the ends of conidiophores and are not enclosed in any

type of structure. Conidia are microscopic in size,

very light-weight, and very dry. The conidia are not

easily wetted and are hydrostatic, tending to associate

with and behave like dust particles. Thus, these spores

are readily spread through the air and are dissemin-

ated on air currents to new surfaces and habitats. If

the spores settle where conditions are favorable for

growth, they rapidly germinate and begin to form a

new mold colony. Sporangiospores are spores that are

produced in an enclosed, sac-like structure, called a

sporangium, at the end of the sporangiophores. These

spores are released into the air when the sporangium

ruptures. Conidia and sporangiospores are common

in the molds found in foods. In addition, individual

molds may form other types of spores, such as

arthrospores, resulting from fragmentation of septate

mycelia, and chlamydospores which result from a

thick wall that develops around individual mycelial

cells. These spores are all referred to as asexual

spores, i.e., they are formed by nonsexual means

and without exchange of any genetic material by

two different molds. Many of the molds that are

important in foods reproduce in this way, without

sexual stages in their life cycles, and are known as

anamorphs. In older literature these are placed in a

group known as the Fungi Imperfecti. These are

molds for which the sexual cycles are unknown.

0004Some of the molds that are important in foods also

reproduce by sexual means in addition to asexual

means. They form, by sexual processes, other types

of spores, including ascospores and zygospores.

These are referred to as teleomorphs (perfect molds,

or the perfect state in older literature), or the teleo-

morphic state. Ascospores are usually formed in some

type of enclosed, sac-like structure located down in

the mycelial mass. These structures are known as asci

(singular: ascus). The asci are enclosed in a fruiting

body called an ascocarp. An ascocarp that is spherical

or flask-shaped and with no opening is known as a

cleistothecium. A spherical or flask-shaped ascocarp

with an opening (ostiole) is called a perithecium. A

saucer or cup-shaped ascocarp that is open is known

as an apothecium. A zygospore is formed when the

tips of two hyphae come together and their contents

fuse. The zygospore develops as a thick-walled struc-

ture between the two hyphal tips. All sexual spores

result from the fusion of two haploid nuclei.

Occurrence

0005Molds are ubiquitous organisms, which literally

means they are found everywhere. The natural habi-

tat of most molds is the soil, where they grow on and

break down decaying vegetable matter. Molds rot

wood, leaves, and other organic debris to form

humus in the soil. During growth on organic debris,

molds form their spores which are readily picked up

by air currents and widely disseminated. When there

is decaying organic matter in an area, there are often

high numbers of mold spores in the atmosphere of

the area. Thus most plant materials, including grains

and seeds, will have a microflora that includes

mold spores. In addition, some grains and seeds

SPOILAGE/Fungi in Food – An Overview 5511

will be colonized by mold while yet in the field, and

these too will become a part of the microflora of

these products. Many of these molds are capable of

growth within the seed under proper conditions.

Molds are therefore common contaminants of food

and animal feed materials, and occur throughout the

environment.

Growth Requirements

0006 Molds can tolerate relatively harsh environments and

adapt to more severe stresses than most microorgan-

isms. Molds require less available moisture for

growth than bacteria or yeasts and can grow on sub-

strates containing concentrations of sugar or salt that

bacteria cannot tolerate. Molds can also grow on

drier substrates than bacteria and can survive in de-

hydrated environments. Molds can tolerate and grow

in high concentrations of acid and over a wide pH

range (2.0–9.0). Since molds are slower-growing than

bacteria and yeasts, the dry or acidic conditions that

inhibit the growth of these organisms, especially

bacteria, flavor the growth of molds. If competitive

growth of bacteria is eliminated by either lower mois-

ture or low pH, mold growth will be enhanced. Thus

mold growth in grains and animal feeds with lowered

moisture content may sometimes occur if the mois-

ture content is not too low. Some molds can obtain

moisture from the atmosphere, as well as the respir-

ation of other organisms, such as insects, and begin to

grow at even low moisture levels. Once mold growth

begins it will probably continue, being fed by

moisture released through its own respiration.

0007 Most molds are highly aerobic, i.e., they require

oxygen for growth, and an abundant supply of

oxygen enhances growth. Carbon dioxide, on the

other hand, inhibits mold growth, and if the carbon

dioxide concentration becomes high enough it can

totally prevent mold growth. Some molds are better

adapted than others to growth in elevated concen-

trations of carbon dioxide. Molds also grow over a

wide temperature range, but most have their optimum

growth temperatures between 25



C and 35



C. Mold

growth is especially rapid under conditions of high

temperatures and high humidity. Some molds can

grow at temperatures as low as 0–5



C and a few

species can even carry on growth processes just

below freezing. A few molds can grow at extremely

high temperatures, even above 60



0008 Molds have simple nutritional requirements. They

can utilize a range of organic substrates, from simple

to complex, requiring primarily a source of carbon

and simple inorganic nitrogen. Molds are capable of

synthesizing their own vitamins and growth factors.

Molds can readily utilize simple carbon sources such

as glucose and other sugars, as well as complex carbo-

hydrates such as starch and cellulose. Molds can also

utilize inorganic nitrogen in the form of nitrate and

ammonium salts, and organic nitrogen such as that

found in proteins, amino acids, and nucleic acids.

Because molds possess a vast array of hydrolytic

enzymes, they are capable of dissimilating and utiliz-

ing a very wide array of substrates. Thus most organic

materials are subject to deterioration by molds if the

conditions of moisture and temperature are not

limiting.

Molds and Food Spoilage

0009Molds are very efficient in converting nutrients into

cell material and mycelial biomass. If a substrate is

composed of nutrients in moderate amounts, most of

the substrate will be converted to cell biomass and

products of primary metabolism for essential life pro-

cesses. If nutrients are available in large or excessive

amounts, a variety of breakdown products may be

excreted into the medium, and storage reserves of

carbohydrates and lipids may accumulate in the my-

celia. At some point in the life cycle of the mold, when

growth slows and conditions are appropriate, the

mold may convert these carbohydrates and lipids to

alcohols, organic acids, and complex heterocyclic

biochemical compounds. This process is known as

secondary metabolism since the metabolites or com-

pounds produced have no apparent purpose in essen-

tial life processes. These ‘secondary metabolites’ may

thus accumulate in the substrate, causing off-flavors

and other problems, including toxicity. The filament-

ous hyphae of the molds are well adapted to growth

over surfaces and through or into porous and solid

substrates. The hyphae provide a large surface area

relative to the mold biomass to excrete enzymes that

break the substrate down into available nutrients,

which in turn are absorbed back into the hyphae.

The nutrients may be transported to the actively

growing hyphal tips, where they are utilized for

energy and to produce primary metabolites and

form new active cytoplasm. The nutrients may also

be used for maintenance of cellular activities, or be

converted to cellular storage reserves and secondary

metabolites.

0010As a result of the metabolic activity of molds in a

substrate, a number of consequences – desirable or

undesirable – can occur. If the substrate is a food or an

animal feed, the biochemical activities of the mold

may result in deterioration and spoilage as the sub-

strate is broken down, and undesirable byproducts

accumulate, causing off-flavors, loss of dry matter

and nutrients, as well as toxicity and other problems.

Particularly in drier substrates, such as grains and

5512 SPOILAGE/Fungi in Food – An Overview

animal feeds, such deterioration will result in spoil-

age. Some of the secondary metabolites of certain

molds are compounds that are toxic to humans and

animals. These toxic substances are collectively

known as ‘mycotoxins.’ (See Mycotoxins: Occur-

rence and Determination.)

Control of Mold Through Processing and

Storage

0011 Mold growth is affected by a number of factors,

including atmosphere, moisture content, relative

humidity, temperature, microbial competition, and

chemicals in the substrate. Since molds are very toler-

ant of acidic conditions, and have few nutritional

requirements, the pH and nutrient content of a sub-

strate cannot be used to affect to any significant

extent the ability of molds to grow.

0012 Moisture and temperature, however, are probably

the two most critical factors affecting mold growth

that can be used as control factors, and it is difficult to

discuss one without the other. The moisture content

of a substrate is less meaningful, in terms of under-

standing the effect of water on mold growth, than

water activity (a

). Water activity has taken the

place of moisture as the most useful expression of

the availability of water for microbial growth. The

of a substrate is defined as the ratio of the vapor

pressure of the substrate to that of pure water. (See

Water Activity: Effect on Food Stability.)

0013 The a

of pure water is 1.0; therefore the a

of any

substrate will be less than 1.0. The a

is a measure of

the amount of water not bound by the substrate, and

which is available to microorganisms for their

growth. The lower the a

, the less water is available

to molds for growth. Moreover, the a

of the sub-

strate is affected by the relative humidity (RH) of the

environment in which the substrate is found. RH

refers to the moisture in the atmosphere surrounding

the substrate, and a

is a property of the substrate and

its moisture content. In a closed system, the a

of a

substrate and the RH of the atmosphere surrounding

it will be in equilibrium. Under equilibrium condi-

tions, the a

of a substrate will be equal to the RH

of the atmosphere surrounding it divided by 100.

Thus the final moisture content of a substrate, i.e.,

food or feed, will depend upon the substrate reaching

equilibrium with the atmospheric RH to which it is

exposed.

0014 The concept of a

is important in understanding

how molds may grow in a seemingly dry substrate.

Conditions such as high humidity or a microenviron-

ment affected by insect respiration can cause the a

a small portion of a substrate to rise to a level that

may permit mold growth. Once growth has been

initiated, respiration of the mold will also contribute

to increasing a

of the surrounding substrate. In this

way the mold growth may become a spreading, self-

perpetuating process, with the pocket of growth

becoming ever larger. This is what causes ‘hot spots’

in a mass of stored grain or animal feed.

0015The minimum a

at which microorganisms associ-

ated with foods and feeds will grow have been studied

extensively. The minimum a

for the general groups

of microorganisms are given in Table 1. Halophilic

bacteria, xerophilic molds, and osmophilic yeasts are

adapted to growth at very low a

. Most spoilage and

toxigenic molds grow over the a

range 0.72–0.94.

Mold growth is completely inhibited at a

values

below 0.65. This would be equivalent to moisture

contents well below 20%.

0016Temperature and a

interact to affect microbial

growth. If temperature is near the optimum growth

temperature of a mold, the range of a

over which the

mold can grow will be greatest, and at any tempera-

ture the ability of a mold to grow will be reduced as

the a

is reduced. Conversely, if the a

of a substrate

is high, molds will be able to grow over a wider range

of temperatures and will be able to grow at lower

temperatures.

0017Atmospheric gases, other than moisture, also affect

mold growth. Molds require oxygen to grow, and are

inhibited by increasing concentrations of carbon

dioxide or decreasing concentrations of oxygen from

those found in air. A concentration of 40% carbon

dioxide in air depresses fungal growth, but the carbon

dioxide level must be increased to more than 90% to

inhibit growth completely. Likewise, reducing the

oxygen content of air to less than 2.0% depresses

mold growth, but to prevent growth the oxygen

level must be reduced to 0.2%. Complete replace-

ment of air with a nitrogen atmosphere will also

inhibit mold growth. Controlled-atmosphere (CA)

storage of commodities has been studied as a measure

of preventing mold deterioration. Both the carbon

dioxide and oxygen concentrations are usually con-

trolled. Controlled atmosphere with 10% carbon

dioxide and 2.0% oxygen greatly increases the time

tbl0001Table 1 Minimum water activity (a

) requirements of micro-

organisms

Microorganism Minimum a

Most spoilage bacteria 0.90

Most spoilage yeasts 0.88

Most spoilage molds 0.80

Halophilic bacteria 0.75

Xerophilic molds 0.65

Osmophilic yeasts 0.60

SPOILAGE/Fungi in Food – An Overview 5513

for mold growth to begin and reduces the amount of

growth. (See Controlled-atmosphere Storage: Appli-

cations for Bulk Storage of Foodstuffs.)

0018 The presence of other microorganisms tends to

restrict fungal growth if conditions are favorable for

the growth of the other microorganisms. Bacteria and

yeasts are capable of more rapid growth than molds

and tend to overgrow molds. The rapid growth of

bacteria on fresh meat, for example, is the probable

reason for the fact that molds are rarely seen growing

on these substrates. Lactic acid bacteria have been

shown to be competitive with molds, and to suppress

mycotoxin production. Molds are also competitive

with each other, and under certain conditions one

mold may prevent the growth of another mold or

may alter its growth patterns and metabolism. Com-

petition by bacteria and yeasts and between mold

species is affected by the microenvironment of the

substrate. The a

, RH, and temperature all have an

impact on competition and growth and will deter-

mine which organism or group of organisms will

predominate. (See Lactic Acid Bacteria.)

0019 Mold growth is also affected by chemicals in the

substrate which have antimicrobial or antifungal

properties. These chemicals may be naturally occur-

ring compounds in the substrate, or they may be

added for the purpose of preservation. Naturally

occurring substrates, such as benzoic acid in cran-

berries, and components of essential oils in herbs

and spices, may restrict or prevent fungal growth.

Mold growth may also be prevented in foods and

feeds by the addition of antifungal or antimycotic

chemicals. These substances may be organic acids

such as sorbic, propionic, and benzoic acids, among

others, or salts of these acids, antibiotics such as

natamycin, chemical dyes such as gentian violet in

the case of poultry feeds, antioxidants, or combin-

ations of these and various other chemicals. In most

cases the levels of the chemicals used are such that

they are fungistatic, i.e., they prevent or delay mold

growth, but do not kill or completely inhibit growth

for an indefinite period of time. Molds are not very

heat-resistant and are readily killed by most thermal

processes, such as cooking, baking, etc. (See Essential

Oils: Properties and Uses; Fungicides ; Preservation of

Food.)

Classification and Specific Genera of

Molds

0020 There are about 100 000 different species of fungi,

although relatively few of these are directly involved

in the deterioration of food and agricultural products,

and/or mycotoxin production in these products.

Genera that are of particular interest because of

their involvement in deterioration of foods and agri-

cultural commodities, and potential mycotoxin

production are as follows: Aspergillus, Penicillium,

Fusarium, Alternaria, Trichothecium and Tricho-

derma. Other genera, important primarily as spoilage

organisms, include Rhizopus, Mucor, and Clado-

sporium. The most significant mycotoxin-producing

molds are considered to be numerous species in the

genera Aspergillus, Penicillium, and Fusarium. Alter-

naria, Trichothecium, and Trichoderma contain a few

individually toxic species that are important. Descrip-

tions of nine of the most common genera of molds

found in foods are given below. The first eight are

septate molds, i.e., the hyphae have cross-walls, while

the last one is representative of nonseptate molds, in

which the hyphae do not have cross-walls.

Aspergillus

0021Aspergillus is a very important genus of molds, very

widespread, with species involved in food spoilage,

mycotoxin production, and fermentations. The A.

flavus–oryzae group contains the species A. flavus

and A. parasiticus, which can produce aflatoxins.

This group also contains A. oryzae, which is nontoxic

and is used in oriental food fermentations to produce

items such as soya sauce and miso. The A. ochraceus

group includes A. ochraceus and other species that

are capable of producing ochratoxins and penicillic

acid. The A. niger group is widespread, and often

involved in food spoilage. A. niger is now known

also to be a producer of ochratoxin. What used to

be called the A. glaucus group is now known as the

anamorph of the genus Eurotium, which includes E.

glaucus and E. repens. These are xerotolerant molds

that can grow on foods that are very dry or contain

high concentrations of sugar or salt. The aspergilli

reproduce by producing conidia, which are produced

on a conidiophore that arises from a special cell in the

mycelium called a foot cell (Figure 1). The entire

conidiophore appears to be a single cell that grows

upright and terminates in a globose, elliptical, or

clavate swelling known as a vesicle. Arising from the

vesicle are bottle-shaped structures called sterigma

(phialides) in which the conidia are produced. The

conidia are pushed out of the end of the sterigma and

remain loosely attached to one another, forming

chains. The colors of the conidia of the aspergilli are

characteristic for different groups and species, and

this is helpful in recognizing the different groups.

Spores of the A. flavus–oryzae group are different

shades of olive-green to yellow-green; spores of the

A. niger group are jet-black to brownish-black to

purple-brown; spores of the A. ochraceus group

range from buff-tan to yellow in color. E. glaucus

and E. repens possess conidia that are some shade of

5514 SPOILAGE/Fungi in Food – An Overview

green, but also produce brightly colored yellow to

reddish cleistothecia. Many Aspergillus species also

produce sclerotia, which are macroscopic, hard,

dense masses of hyphae that appear as small, dark-

colored masses in the mycelia. Aspergillus species

often occur in grains, nuts, oil seeds, and on certain

types of dry cured meat.

Penicillium

0022 Penicillium is also a widespread genus that is import-

ant in foods. Penicillium species contaminate a wide

variety of foods and are capable of growing at

refrigeration temperatures. Thus they often spoil

refrigerated foods, especially cheese. They are also

common on grains, breads, cakes, fruits, preserves,

cured and aged hams and sausages, and in the

spoilage of certain fruits. The penicillia produce co-

nidia from conidiophores that branch near the apex,

forming a brush-like structure or penicillus (Figure 2).

At the apex of the conidiophore are somewhat en-

larged cells known as metulae. From the metulae arise

the sterigma or phialides. It is in these structures that

the conidia are produced and pushed out in chains.

The conidia of the penicillia are colored, but mostly in

shades of gray to blue to blue-green. The colors

are not as distinctive for the various species as

for the aspergilli, and are therefore not as helpful in

the identification of species. Some species form

ascospores in cleistothecia and are also placed in the

teleomorphic genera of Talaromyces or Eupenicil-

lium. There are a number of important Penicillium

species. P. verrucosum, P. viridicatum,andP. auran-

tiogriseum are common in grains and some can also

occur on cheese. They can produce a number of

mycotoxins, including ochratoxin, penicillic acid,

and others. P. martensii, a synonym for P. aurantio-

griseum, has been found growing in high-moisture

corn and can produce penicillic acid. P. expansum

causes rots of fruits, especially apples, and produces

patulin. P. digitatum, with green-colored conidia,

causes soft rot of citrus fruit, usually at ambient tem-

peratures, whereas P. italicum, which has blue spores,

causes soft rot of citrus at refrigerated temperatures.

P. roqueforti has blueish-colored conidia and is used

in the ripening of blue-veined cheeses. However, wild

types of P. roqueforti often occur in dairy environ-

ments and also contaminate other types of cheeses,

such as Cheddar and Swiss, and grow and cause

spoilage under refrigerated storage. P. camemberti

produces grayish spores, and is used for surface

ripening of Camembert and Brie cheeses. Many

other Penicillium species are known to produce vari-

ous toxic substances, many of which also have antibi-

otic properties, but appear to be too toxic for

therapeutic use. The most famous antibiotic, penicil-

lin, which has been used to cure countless bacterial

infections, is produced by P. notatum.(See Cheeses:

Chemistry and Microbiology of Maturation.)

Conidia

Vesicles

Stipes

'Foot cells'

Metulae

Sterigma

(phialides)

fig0001 Figure 1 Conidiophores characteristic of Aspergillus species,

showing a single layer of phialides or sterigma (uniseriate) and

double layer of cells, phialides and metulae (biseriate). Adapted

from Klich MA and Pitt JI (1988) A Laboratory Guide to the Common

Aspergillus species and Their Telemorphs. North Ryde, Australia:

Commonwealth Scientific and Industrial Research Organization.

Conidia

Phialides

Metulae

Ramuli

Rami

Stipe

fig0002Figure 2 Examples of the simplest and most complex conidio-

phores produced by Penicillium species. Adapted from Pitt JI

(1988) A Laboratory Guide to Common Penicillium Species, 2nd

edn. North Ryde, Australia: Commonwealth Scientific and Indus-

trial Research Organization.

SPOILAGE/Fungi in Food – An Overview 5515

Fusarium

0023 Fusarium species are capable of growing on stored

foods, but more commonly occur in the field, where

they infect grain plants and may also invade the

grain itself. Fusarium colonies on agar appear to

be cottony owing to dense growth of white hyphae.

They produce various pigments, with colors ranging

from white, through pink, salmon-pink and carmine

red, to purple. Some species also produce yellow

and brown pigments. Fusarium species produce

septate, curved to crescent or sickle-shaped conidia,

called macroconidia which are, to some extent,

characteristic of species (Figure 3). The macroconi-

dia are slightly curved and tapered towards each end

(fusiform) and are sometimes also referred to as

boat-shaped. In some species the apical cell of the

macroconidium is elongated and the basal cell,

where the conidium was attached, is shaped like a

foot cell. In addition, some species also produce

smaller, one- or two-celled conidia known as micro-

conidia. The microconidia may be pear-shaped

(pyriform), fusiform or ovoid, and straight or

curved.

0024 Fusarium species are widely distributed throughout

the world, in both temperate and tropical regions.

They are found in the soil, especially cultivated soils,

and actively degrade organic matter in the soil. Many

species are also considered to be plant pathogens,

capable of causing a range of plant diseases such as

root and stem rots, blights, and wilts. Two plant

diseases that occur in the field, but which affect

grain quality and safety, are wheat scab, also called

Fusarium head blight, and ear rot in corn (maize).

One of the species involved in both of these condi-

tions is F. graminearum, which invades the grain

(wheat or corn) in the field and produces deoxyniva-

lenol (DON), also called vomitoxin. F. graminearum

is most common in North America, whereas a closely

related species, F. culmorum, is more common in

Europe. F. graminearum and F. culmorum also pro-

duce zearalenone. F. verticillioides (moniliforme)

produces fumonisins and other metabolites in corn,

as does F. proliferatum. F. proliferatum and F. sub-

glutinans also produce moniliformin and other com-

pounds. Other species can also invade grains and

produce other toxins. Fusarium species can also

invade fresh fruits and vegetables during storage,

causing various rots and spoilage.

0025Some of the Fusarium species have a sexual stage

and are placed in the teleomorphic genera of Gibber-

ella, Nectria, Calonectria, and Plectoshaerella. For

example, the telemorph of F. graminearum is Gibber-

ella zeae. Fusarium species are very important as

plant pathogens and as potential mycotoxin-

producing organisms. They can therefore cause both

spoilage and safety problems in foods, especially

cereal grains and foods containing cereal products.

(See Cereals: Dietary Importance.)

fig0003 Figure 3 Macro- and microconidia typical of the genus Fusarium. Reproduced from Spoilage: Fungi in Food – An Overview. En-

cyclopaedia of Food Science, Food Technology and Nutrition, Macrae R, Robinson RK and Sadler MJ (eds), 1993, Academic Press.

5516 SPOILAGE/Fungi in Food – An Overview