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

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of vegetable and animal trans-fatty acids was evident.

In a fifth analysis based on the cohorts of the Seven

Countries Study, initially studied in the late 1950s

and early 1960s, the intakes of both saturated fatty

acids and C18:1 trans-fatty acids showed significant

statistical associations with the 25-year CHD mortal-

ity. This study was based on analyzed average diets

and individual data were not available. In 14 out of

the 16 study cohorts, trans-fatty acids were mainly

derived from animal products. The results thus repre-

sent rather the effects on CHD risk of concomitant

saturated fatty acids, present in far higher amounts in

the main animal sources of trans-fatty acids, than the

relatively small amounts of trans-fatty acids present

in these foods.

0010 It has been calculated from the combined results of

the cohort studies that a decrease in trans-fatty

acid intake by 2% of energy decreases the risk of

CHD by 25%. This would correspond roughly to

the effect of a reduction of 5% of energy in the intake

of saturated fatty acids. A reduction of 2% of energy

in trans-fatty acid intake is seldom possible, because

the current average intakes of trans-fatty acids are

below 2% of energy in most countries, but a reduc-

tion of saturated fatty acid intake from 15 to 10% of

energy would be feasible in most western countries.

Mechanisms of Action of

Trans

-Fatty

Acids

0011 The effects of trans-fatty acids on serum lipoproteins

clearly have a mechanism that is different from that of

saturated C12–16 fatty acids. Both increase the LDL-

cholesterol concentration in serum but, in addition,

saturated fatty acids increase serum HDL-cholesterol

concentration, whereas trans-fatty acids decrease the

HDL-cholesterol concentration. The effect of trans-

fatty acids may also appear more slowly, within 3–6

weeks, than that of saturated fatty acids that becomes

apparent in 2–3 weeks’ time.

0012 An increase of the cholesterol ester transfer protein

(CETP) activity by trans-fatty acid feeding has been

documented in several but not all human intervention

studies with trans-fatty acids. CETP transfers

cholesterol from HDL to very-low-density lipopro-

tein (VLDL) and LDL. Increased CETP activity

could thus explain the decrease in serum HDL-chol-

esterol concentration combined with an increase in

LDL-cholesterol found in intervention studies with

trans-fatty acids. This could also explain the negative

findings in many animal studies, since mice, rats, and

pigs do not exhibit CETP activity. The increase in

lipoprotein a (Lp(a) ) found in most trans-fatty acid

supplementation studies is another difference be-

tween the effects of saturated and trans-fatty acids.

Lp(a) levels are mainly genetically determined, and

the mechanism of the effect of trans-fatty acids on

LP(a) levels remains unexplained.

0013In experimental studies on the effects of fatty acids

in isolated mouse islets of Langerhans, trans-fatty

acids increased maximal insulin output compared

with the corresponding cis-isomers. In human studies,

no clear effects on insulin sensitivity by trans-fatty

acids have been observed.

0014The effects on hemostatic variables have been

measured in two intervention trials. No effects on

fibrinogen, factor VII, or tissue plasminogen activator

levels, ascribed to trans-fatty acids, could be ob-

served. In one of the studies, plasminogen activator

inhibitor-I (PAI-I) antigen and activity were increased

by the consumption of partially hydrogenated vege-

table oil, but this finding was not confirmed by the

other study. As far as blood coagulation and fibrino-

lysis are concerned, there seems to be little difference

between the effects of saturated and trans-fatty acids.

0015Trans-fatty acids compete with linoleic acid and

alpha-linolenic acid for the metabolizing enzymes.

In experimental animals they impair the microsomal

desaturation and elongation of the essential fatty

acids to their long-chain metabolites arachidonic

acid and docosahexaenoic acid. It has been suggested

that trans-fatty acid intake of the mother during preg-

nancy and lactation may be harmful for premature

and newborn babies, because a high trans-fatty acid

intake may impair the formation of the essential long-

chain polyunsaturated fatty acids in the baby. In

adults with ample consumption of polyusaturated

fatty acids, this effect of trans-fatty acids is probably

without practical importance.

Trans

-Fatty Acids and Cancer

Experimental Studies

0016There is much information from animal studies con-

cerning the effects of different fatty acids on experi-

mental cancer, but very few of these yield information

on the effects of trans-fatty acids. In two studies in

mice comparing elaidic acid (trans-9 C18:1) as pure

fatty acid with esterified oleic acid in triglycerides,

a possible tumor-promoting effect of elaidic acid

was observed. Subsequent studies comparing trans-

and cis-isomers esterified in triglycerides have shown

quite similar effects of trans- and cis-monoenoic fatty

acids on the development of experimental colon

cancer and breast cancer.

Epidemiological Studies

0017It is difficult to assess the effects of dietary trans-fatty

acids independently of the intakes of the much more

2328 FATTY ACIDS/

Trans

-fatty Acids: Health Effects

abundant saturated and cis-unsaturated fatty acids.

Therefore, data on trans-fatty acids have not been

reported in the majority of the studies. Most studies

on the associations between dietary fatty acids and

risk of cancer have addressed breast cancer. In the

largest of the cohort studies, the Nurses’ Health

Study, no association between the intake of trans-

fatty acids and risk of breast cancer was observed.

In some case-control studies the fatty acid compos-

ition of adipose tissue or serum has been used as a

biomarker of intake. In two of these, no association

was found between trans-fatty acids and the risk of

breast cancer. In a third study, trans-fatty acids were

associated with an increased risk of breast cancer in

the lowest tertile of polyunsaturated fatty acids. In

one study, a significantly lower proportion of trans-

11 C18:1 (trans-vaccenic acid), mainly derived from

cheese, was found in postmenopausal women with

breast cancer as compared with matched healthy con-

trol subjects, but the trans-9 and trans-10 isomers in

serum showed no association with the risk of breast

cancer.

0018 Intake of fatty acids has been associated with the

risk of colorectal cancer in some prospective studies,

but the contribution of trans-fatty acids to the risk has

not been assessed in any of the studies. Based on these

scanty data, it can be concluded that available evi-

dence does not suggest any appreciable role to the

intake of trans-fatty acids in relation to the risk of

any type of cancer.

Future Aspects

0019 In the past, high intakes of trans-fatty acids,

exceeding 4% of energy intake, have been recorded

in some countries like Norway and the Netherlands,

due to the consumption of hydrogenated vegetable

and fish oils, and in Canada and the USA, due to

common use of partially hydrogenated vegetable oils.

As awareness of the undesirable effects on serum

lipoproteins of partially hydrogenated vegetable and

fish oils has increased, table margarines and other

soft spreads containing no or low concentrations of

trans-fatty acids have become commonly available

but industrial shortenings and fats for deep-frying

remain high in trans-fatty acids. For reasons of tex-

ture, e.g., in icecream and leafy pastries, or stability,

e.g., in deep-frying and in industrially produced fatty

foods with a long shelf-life, trans-fatty acids or satur-

ated fatty acids or both will be used in these foods

even in the future. In cooking and baking at home,

hard fats can be replaced by vegetable oils, but it

seems advisable to restrict the consumption of

industrially manufactured fatty foods because of

their undesirable fatty acid composition. If and

when trans-fatty acids are removed from foods, as

much as possible they should be replaced by cis-un-

saturated fatty acids. If saturated fatty acids are sub-

stituted for trans-fatty acids, the benefit in terms of

CHD risk is questionable.

0020The proportion of trans-fatty acids derived from

ruminant animal products will increase concomi-

tantly with the reduction of trans-fatty acids derived

from partially hydrogenated vegetable oils in foods.

Already in 1995, dairy products and meat contrib-

uted more than 50% to total trans-fatty acid intake in

seven out of the 14 European countries participating

in the TRANSFAIR study. It is possible to substitute

trans-vaccenic acid and CLA for saturated fatty acids

in milk and beef fat by modifying the feeding of cows.

So far there are no studies indicating whether modi-

fying the composition of milk fat in this way should

be considered beneficial or harmful with respect to

effects on CHD risk factors.

See also: Cancer: Diet in Cancer Prevention; Cholesterol:

Factors Determining Blood Cholesterol Levels; Coronary

Heart Disease: Etiology and Risk Factor; Lipoproteins

Further Reading

Almendingen K, Jordal O, Kierulf P, Sandstad B and Ped-

ersen JI (1995) Effects of partially hydrogenated fish oil,

partially hydrogenated soybean oil, and butter on serum

lipoproteins and Lp[a] in men. Journal of Lipid Research

36: 1370–1384.

Aro A (1998) Epidemiological studies on trans fatty acids

and coronary heart disease. In: Se

dio JL and Christie

WW (eds) Trans Fatty Acids in Human Nutrition, pp.

235–260. Dundee: Oily Press.

Aro A (2001) Complexity of issue of trans fatty acids.

Lancet 357: 732–733.

Aro A, Kardinaal AFM, Salminen I et al. (1995) Adipose

tissue isomeric trans fatty acids and risk of myocardial

infarction in nine countries: the EURAMIC study.

Lancet 345: 273–278.

Ascherio A, Hennekens CH, Buring JE, Master C, Stampfer

MJ and Willett WC (1994) Trans-fatty acids intake and

risk of myocardial infarction. Circulation 89: 94–101.

Hu FB, Stampfer MJ, Manson JE et al. (1997) Dietary fat

intake and the risk of coronary heart disease in women.

New England Journal of Medicine 337: 1491–1499.

Ip C and Marshall JR (1996) Trans fatty acids and cancer.

Nutrition Review 54: 138–145.

Katan MB, Zock PL and Mensink RP (1995) Trans fatty

acids and their effects on lipoproteins in humans.

Annual Review of Nutrition 15: 473–493.

Kris-Etherton PM (ed) (1995) Trans fatty acids and coron-

ary heart disease risk. American Journal of Clinical

Nutrition 62: 655S–707S.

Lichtenstein AH (1997) Trans fatty acids, plasma lipid

levels, and risk of developing cardiovascular disease.

Circulation 95: 2588–2590.

FATTY ACIDS/

Trans

-fatty Acids: Health Effects 2329

Oomen CM, Ocke

MC, Feskens EJM et al. (2001) Trans

fatty acid intake is associated with an increased 10-year

risk of coronary heart disease in the Zutphen Elderly

Study. Lancet 357: 746–751.

Pietinen P, Ascherio A, Korhonen P et al. (1997) Intake of

fatty acids and risk of coronary heart disease in a cohort

of Finnish men. The alpha-tocopherol, beta-carotene

cancer prevention study. American Journal of Epidemi-

ology 145: 876–887.

Precht D and Molkentin J (1995) Trans fatty acids: implica-

tions for health, analytical methods, incidence in edible

fats and intake. Die Nahrung 39: 343–374.

FDA See Food and Drug Administration

FERMENTED FOODS

Contents

Origins and Applications

Fermented Meat Products

Fermentations of the Far East

Beverages from Sorghum and Millet

Soy (Soya) Sauce

Origins and Applications

B J B Wood, University of Strathclyde, Glasgow, UK

Introduction

0001 Many entries in this Encyclopedia will deal, directly

or indirectly, with the actions of microorganisms of

foodstuffs. Some will be entirely negative, relating to

food poisoning, disease transmission, and toxin pro-

duction. Others will show that changes effected by

microbes can be beneficial and even desirable, bring-

ing about changes that enhance the texture, flavor,

color, edibility, and hence the value of the foodstuff

concerned. This entry discusses the benefits and prob-

able origins of the fermentations. It further attempts

to place them in a historical and economic context.

The Beginnings of Food Fermentation

0002 Although we cannot know how or when the practice

of fermentation in relation to food began, all avail-

able evidence suggests that it is a very ancient part of

human development. In fact, fermentation can be

seen as a subset of biodeterioration. All things that

can serve as foods for humans (or any other animal)

are, by their capacity to act as foods, more or less

unstable. If they are food for mammals, then they will

also be able to support the life of many types of

bacteria and molds. In practice, even such apparently

stable materials as wood are open to attack by

microbes and insects. There is a powerful drive

throughout nature to use the energy and nutrition

present in organic materials, eventually mineralizing

these materials back to carbon dioxide, water, and

simple mineral salts.

0003We see attack by such microorganisms as, primar-

ily, a deterioration, or loss of desirable characteristics.

Some such changes, however, turn out to have

desirable characteristics. Such changes may produce

improvements in flavor, odor, and texture. In add-

ition, there is substantial evidence of improvements

in nutritional status and value arising from controlled

fermentations. Various studies have shown that even

simple fermentations of basic cereal grains with the

indigenous (mainly lactic acid bacteria) microflora

generate significant increases in the levels of some

B-group vitamins. There are strong suggestions that

plant proteins, which are somewhat difficult for the

monogastric digestive system to handle, can be made

more digestible through the actions of proteolytic

enzymes produced by bacteria and fungi. Many adults

are intolerant to lactose, the principal sugar of milk,

but fermentations such as that to produce yogurt

reduce or eliminate this problem. Fermentations can

2330 FERMENTED FOODS/Origins and Applications

also reduce or remove toxins and other ‘antinutri-

tional factors.’ Perhaps the most important example

of the former is the detoxification of cassava, while an

example of the latter is hydrolysis of phytic acid, with

removal of sequestering by it of divalent metals. Per-

haps even more significant in the present context may

be the prospect that fermentation increases the stabil-

ity of the affected food, increasing its resistance to

attack by other organisms. Before the advent of

modern methods for food preservation, such as freez-

ing and canning, even a short extension in storage life

would be precious. The prolonged storage possible

for the main protein in milk (casein) consequent upon

conversion to a hard cheese (such as Cheddar) would

thus be of immense value. We must also remember

that availability evenly spread through the year is a

very modern phenomenon. In any given region (par-

ticularly in the temperate parts of the world) food

supply is very seasonal. The idea that tomatoes,

apples and new potatoes would always be on sale

would have seemed unreasonable even a couple of

decades ago. Now it is taken for granted throughout

the industrialized world.

An Example

0004 The existence of small pits (perhaps a meter cube, or

even less) dug into the chalk of southern England has

long been known, but their purpose remains a matter

for controversy. One suggestion has been that they

would have been used to store grain. However,

a priori this seems unlikely. In the ground grain will

be exposed to moisture. All seeds will take up avail-

able water as a preparation for germination, and will

then become more easily attacked by molds than the

dry seeds would be. Chalk, being very porous, will

readily conduct water. Thus grain storage in pits

dug into the surface of chalk would seem to be an

inappropriate method for conserving the material.

However, experiments showed an interesting

sequence of events. Dry grain was packed into pits

prepared for the purpose, and the pits were then

sealed with a cap of clay or other impervious mater-

ial. Initially, the grain closest to the clay took up

water and was then colonized by a range of fungi

and other microorganisms. Eventually this agglomer-

ation of grains and hyphae formed an impervious

layer, preventing further ingress of moisture. In add-

ition, respiration by the stored grain and the microbes

feasting in the outer layers of the stored material used

up the available oxygen, replacing it with carbon

dioxide. Thus, at the sacrifice of the outermost layer

of the stored material, the bulk of it was preserved for

a long time.

0005 This does not correspond with our normal idea of a

food fermentation. However, it has illustrations for a

number of key points. The pit makers could have had

no understanding of the processes at work in their

pits. Despite this, the prevailing conditions favored

growth of microbes in a beneficial way. There was

some loss of stored material, but this was an accept-

able price for the storage of the rest in useable condi-

tion. All of the foregoing is speculation; we can have

no certain knowledge of how the pits were used by

their makers. The grain storage hypothesis is never-

theless a valid one, and experiments show that the

pits would operate as conservation devices.

Historical Background

0006Very often our understanding of how a fermentation

began is speculation based on our interpretation of

the modern process in the light of our knowledge of

conditions in the past. Sometimes this is aided by

ancient records, pictures such as those from Egyptian

tombs, continuing oral traditions, but in many cases

such evidence is scanty or entirely absent. Thus there

is a great deal of guesswork in our attempts to recon-

struct how particular fermentations originated. In

most cases this is unimportant, but it can be irritating

when we are faced with a product such as kefir. Here

the fermentation relies upon structures called grains.

Modern analyses show that these grains are highly

structured arrangements of yeasts and bacteria upon

polysaccharide membranes. These organisms can be

separately cultivated in the laboratory, but they do

not reform into the characteristic kefir grains when

cultured together. How did the grains arise? Was this

a single event, or did it happen several times (kefir

is widespread across Russia and Eastern Europe)?

Clearly, we are unlikely ever to know the answers to

such questions. Even in simpler cases, such a bread

making or the conversion of grapes to wine or grain

to beer, we have no records showing the beginnings of

such activities. Often there are myths showing such

knowledge as gifts from gods or other superior intelli-

gences. Also foods such as bread and wine frequently

have a place in sacramental activities. The giving and

consumption of bread and wine, central to the Chris-

tian Eucharist, are also found in older traditions,

associated with the Roman gods, for example. This

infers the great importance of such activities at the

change from hunter/gatherer economies to the begin-

nings of settled agriculture. I suggest that this know-

ledge was an essential part of that change. The ability

to store foods enhanced survival over winter and

other periods of hardship.

0007Converting dry grains and other seeds into some-

thing more appetizing than a gruel must have made

agriculture more attractive and valuable. Alcohol,

despite its dangers, provided (and still provides), in

reasonable moderation, a basis for social interaction.

FERMENTED FOODS/Origins and Applications 2331

The apparent changes in the nature of consciousness

effected by alcohol must have had spiritual signifi-

cance, and the economic power possessed by those

who control its production and distribution remains

important to this day. The vital part played by bread

in the agrarian economies of Europe is made starkly

plain by the draconian laws controlling the activities

of medieval bakers, and that of beer by ordinances

such as the German beer laws. The trade in fish sauces

throughout the Roman Empire affords another

example. We tend to associate fish sauces with the

Far East, but it is known that several fish sauces have

been produced in the Mediterranean region since an-

cient times. Archeological evidence indicates that

these products were traded in substantial amounts

throughout the Empire, even as far as Hadrian’s

wall. Although we cannot know for certain their

nature, it seems clear that these were important

condiments in the Roman kitchen.

Options for Food Preservation

0008 Before the advent of bottling, canning, and other

methods using a combination of heat and an effective

seal against recontamination of the heat-treated food

by microbes, there were very few safe technologies

available. Cold was recognized as valuable in de-

laying the onset of putrefaction, but was not generally

available for most of the year. The richest people had

ice-houses, insulated structures where the winter’s

snow and the ice from pools could be conserved for

at least part of the warmer months, then used to store

food, as well as providing the means for preparing

cold drinks. Access to such ice-stores was only for the

very rich, and zero Celsius is of limited value in food

preservation. Despite this, preservation of food in ice

attracted the interest of the great Sir Francis Bacon,

who died in 1626 from a cold caught as a conse-

quence of experiments in preserving fowl with ice.

The discovery that ice mixed with salt gave lower

temperatures was of very limited value, and must

have been an extremely expensive option.

0009 For most people, the main technologies depended

upon reducing the water available for microbial

growth. Air-drying is still important in preserving

many foods in tropical countries, and even in north-

ern latitudes the drying of fish was important. In

practice, such drying is normally accompanied by

some microbial growth, frequently demonstrated by

the odors emanating from the drying food, particu-

larly fish. Salting is a very ancient practice, its import-

ance demonstrated by salt taxes, the Roman payment

of salt to soldiers (hence ‘salary’), and so forth.

Sugar also has importance, principally, although not

entirely, in preserving fruits and some vegetables.

Their naturally dry state confers particular value on

seeds, even though they can be fairly uninteresting

foods without considerable processing. On the other

hand some potential foods, such as cassava (Manioc

esculenta) contain such powerful natural preserva-

tives that they are lethal if consumed in their natural

state, while others, such as millet, contain unaccept-

able levels of tannins or other bitter principles.

0010Thus, the preservative properties associated with

some food fermentations must have been important

even at the dawn of agriculture, and became much

more so as urban civilization developed. Equally, the

abilities of fermentations to detoxify things such as

cassava are essential if these materials are to become

suitable for human consumption. Another preserva-

tive agent derived from fermentation, vinegar, has not

been mentioned so far. Its value as both a condiment

and a preservative has, however been recognized

since the most ancient times. It also had importance

in medicine and healing. With the rapid transfer of

the British population from a mainly rural existence

to an increasingly urban one, consequent upon the

Industrial Revolution, the enhanced demand for vin-

egar resulted in development of the ‘quick’ vinegar

process to replace the slow Orleans method. It must

also be recognized that fermentation often went to-

gether with other methods of preservation, in order to

give the desired results. In particular the capacity of

salt, even at fairly low concentrations, selectively to

enhance growth of certain lactic acid bacteria (LAB)

is vital to the success of important vegetable and meat

fermentations. The possible significance of essential

oils and other factors derived from herbs and other

flavorings will be considered below.

Physical and Chemical Properties of Raw

Materials for Fermentations

0011Appropriate fermentation techniques for given prod-

ucts will be strongly influenced by the physical and

chemical properties of the raw materials to be used in

its preparation. It is therefore useful to attempt a

classification of raw materials. What follows will be

entirely pragmatic, and is not intended as a formal

classification scheme. Instead it will be a grouping by

the characteristics most relevant to fermentation pro-

cedures. In order to do this, it is first desirable to

review the relevant physical and other characteristics.

0012Of the physical properties, probably the most im-

portant will be the availability of water, as this will

strongly influence the types of organisms whose

growth can be supported on a particular medium,

and, in the extreme case, whether any organisms at

all will grow on the material in question. Water avail-

ability can be limited by simple physical dryness,

2332 FERMENTED FOODS/Origins and Applications

i.e., the actual absence of water, and by osmotic pres-

sure creating a physiological drought. Salt and/or

sugar in foodstuffs most commonly induce the latter.

It should be noted that quite low concentrations of

salt, well below that which might be expected to

induce osmotic stress, can strongly influence the

course of fermentations. The structures of some fruits

and vegetables are remarkably well developed to

resist attacks by both plant and microbial invaders.

The cassava tuber affords a particularly highly de-

veloped example of combined physical and chemical

defenses. It has both a tough, fibrous exterior, and a

capacity to produce toxic levels of hydrogen cyanide

when it is damaged. Such materials require to be

mechanically damaged to breach the outer layers.

This is generally accomplished by chopping, shred-

ding, or slicing, depending on the material and

intended product. The outermost layers may also

need to be removed, being tough, fibrous, and lacking

in nutritive value. Where toxins are present (as in

cassava), measures to neutralize them will also be

required. In some cases, however, agents developed

by the plant as protection may be desired in culinary

practice. Examples include the irritants present in

onions and the roots of plants such as radishes.

While stress has been placed on roots, tubers, and

bulbs in the foregoing discussion, arising from their

greater numbers of types, certain other structures also

perform in similar manners. Perhaps the most obvi-

ous example is the cocoa fruit. This is a robust struc-

ture with a tough outer layer, which must be breached

before the inner pulp can undergo fermentation both

to release and chemically modify the seeds that will

yield cocoa powder after roasting and grinding.

0013 The chemical composition of the fermentable ma-

terial is obviously of overriding importance in deter-

mining the types of organisms that can grow on it and

the outcomes of fermentations which they effect. In

some cases there will be ample supplies of (for

example) sugars to give desired levels of organic

acids, B-group vitamins to support growth of fastidi-

ous LAB, and amino acids. In many cases, however,

there will be insufficient readily usable material.

Then, organisms which can produce and export

appropriate hydrolytic enzymes (amylases or prote-

ases, for example) will be at an advantage. They may

also prepare the way for later growth of less compe-

tent organisms such as yeasts and LAB.

0014 The part played by chemicals in herbs, onions, and

garlic can be particularly interesting. We value these

materials principally as flavors in foods, but many of

them also have long traditions as healing agents

and medicinals. There is increasing evidence that

these traditions have a secure basis in scientific fact.

claims that onions, garlic, and many culinary herbs

are powerfully inhibitory against bacteria associated

with food poisoning have been reviewed; it is

reported that onions, garlic, allspice, and oregano

‘killed every bacterial species tested.’ These are

clearly valuable properties if shown to apply to actual

foodstuffs, but an interesting question arises. Many

fermented foods use onions, garlic, and various herbs.

Some sausages use particularly high levels of garlic

(e.g., salami). Sausages are harsh environments even

without these inhibitors. Yet bacteria, such as species

of Carnobacterium and Micrococcus, are present in

these products, and are thought to be essential for

flavor development. How selective is the toxicity of

these plant products? There are clearly interesting

biochemical challenges here, even if these claims

were shown to be fully justified in the field, i.e., in

actual food fermentations. It has been pointed out

that, for example, salamis, although particularly

heavily spiced with garlic, have been associated with

serious illness due to Escherichia coli. Thus claims of

this type need to be assessed very carefully, with

purely laboratory studies and robust trials in actual

foods being run in partnership with each other, if the

effects on food microflora of herbs and spices are to

be fully understood.

0015The foregoing is not intended as a complete discus-

sion of the issues involved here. Rather it is an indica-

tion of some of the factors that require consideration

when attempting to understand the factors influen-

cing the initial development and subsequent evolution

of food fermentations.

A Classification of Raw Materials

Animal Products

0016Meats This term is taken to include the flesh from

mammals, and also that from fishes, birds, and crust-

aceans. In all cases, the material as obtained post-

mortem is usually in the form of chunks of tissue,

dissected organs (such as muscles, liver), whole or-

ganisms (often, but not always eviscerated; small fish

are an obvious example). Occasionally the material

may be comminuted in the course of its extraction,

but relatively large pieces are more usual. Sometimes,

particularly in small fish for conversion to fish sauce

or for fermentation with rice, the material can be used

without further physical modification. More usually

it is necessary to comminute the material by mincing

or grinding. This is primarily to insure sufficiently

intimate mixing of salt, spices, farinaceous materials,

and other additives that both promote the desired

fermentation and confer desired texture and flavor

on the finished product. It also simplifies packing

the prepared mixture into appropriate casings.

FERMENTED FOODS/Origins and Applications 2333

0017 In certain cases the raw material may be of rela-

tively low intrinsic value, with fermentation being a

way of utilizing residues. Typical of this situation is

producing oriental fish sauces from trash fish and

the viscera, heads, tails, and other unwanted parts

remaining after marketable fish has been prepared

for sale. For high-value products, such as quality

sausages, producers will specify the meat carefully,

with prime cuts being essential for the best products,

although sausages can represent a way of using lesser-

quality meat economically, while still yielding a

merchantable product.

0018 Milk Milk is surely the archetype for a fermentation

substrate. Its production, particularly by traditional

methods, guarantees that it carries a substantial mi-

crobial load ab initio. Even in modern parlors using

mechanical milking and strict hygiene, the milk still

has a significant number of microbes in it. The

high water content, presence of readily fermentable

carbohydrate (lactose) and nitrogenous materials,

B-vitamin content, and the near-neutral pH combine

to provide nearly ideal growing conditions for a wide

variety of organisms, including potential pathogens.

The temperature of freshly drawn milk is also near

the optimum for many bacteria. Thus modern pro-

cessing, for direct consumption, butter production

or fermentation, requires rapid cooling of the milk,

swift transport to a processing center, and rapid ther-

mal processing (usually pasteurization or ultrahigh-

temperature (UHT) treatment) to provide a safe and

relatively stable product. Despite impassioned argu-

ment about the greater flavor claimed for cheeses

made from unpasteurized milk, some developed

countries continue to insist on appropriate heat treat-

ment for all milk to be used for making cheeses. On

the other hand it must be acknowledged that the

bacteria in unpasteurized milk tend to be predomin-

antly LAB, and that the selected cultures employed in

modern production originate from isolates originally

found in spontaneous fermentations. The relatively

anaerobic conditions, which develop in bulk milk,

rapid acidification and various factors elaborated by

LAB (bacteriocins, hydrogen peroxide) combine to

suppress the growth of many pathogens in cheeses.

Thus cheese and yogurt production are still valid

technologies for societies where modern milk process-

ing is not available to most of the producers.

Plant Materials

0019 The great diversity of plant materials means that any

attempt at grouping into classes will be fraught by

difficulties caused by overlaps and ambiguities. For

example, tomatoes and cucumbers, although obvi-

ously fruit, are often placed among the vegetables,

while the edible stems of rhubarb are placed alongside

fruits. Thus, what follows is entirely arbitrary, reflect-

ing the practical problems in fermenting plant foods.

0020Leafy material Grass and other forage materials are

converted into silage on an enormous scale as an

essential part of modern ruminant farming. Although

not normally thought of as a food fermentation, i.e.,

not part of the human diet, this is probably the most

important among leaf fermentations in the wider

context. Among materials for direct human consump-

tion, the best-known products are kimchi and sauer-

kraut. The latter is a highly industrialized process in

the major producing nations. Undoubtedly it was

developed principally as a storage process for con-

serving excess cabbage through the winter in areas

where the severe winter weather would destroy

cabbage heads left in the fields, while cut heads

would quickly deteriorate in store if held as the un-

modified material. The key factors for fermentation

are provided for by adding about 2–3% by weight of

salt to shredded cabbage heads, then packing tightly

into containers where the sap, withdrawn from the

plant tissue by osmotic action of the dissolving salt,

quickly displaces remaining air from between the

plant material. Bacteria naturally present on the

plant surfaces drive the lactic fermentation, although

there is a tendency towards using selected cultures

now. This simple process gave a product that could

be conserved without deterioration for many months,

even in the absence of refrigeration. Obviously there

is no need to continue this process as a means for

conserving cabbage in industrialized societies, where

advanced storage systems and transportation which

can deliver any food from any part of the world

without regard to season provide complete freedom

from the old domination by the solar cycle. However,

this has not reduced demand for the fermented prod-

uct. On the contrary, those accustomed to it have

taken its production with them when they have mi-

grated to and settled in other parts of the world.

Consequently its production is, if anything, increas-

ing. The technology is basically the same as for the

materials discussed in the next section, with the key

difference that they use salt in prepared brine,

whereas here dry salt is added to the raw material.

0021Fruits Cucumbers are perhaps the classical example

here, although olives would be cited first in Mediter-

ranean climates. Other examples include tomatoes.

Small onions and certain types of radish roots, al-

though not fruits, are processed in the same way.

Again the technology is very simple, easily applicable

on a village or domestic level, and originally a way of

conserving seasonal surpluses of produce against

2334 FERMENTED FOODS/Origins and Applications

winter shortages. Essentially the prepared material is

immersed in a salt solution (brine) and a spontaneous

lactic fermentation develops. In reasonably cool

conditions the products are stable during prolonged

storage. The observations about the survival of sauer-

kraut technology after the conservation need had

passed apply with equal force here, as do those on

industrialization of the processes. Olives are remark-

able in the market penetration that the fermented

product has achievedoutside itstraditional consumers.

0022 Another type of conservation of fruits relies on

fermenting the released juices to produce stable

liquids. This is a very pedestrian way of describing

the delights of wines and the products from apple

(cider; USA ‘hard cider’) and pear (perry) juices,

but is deliberately done to place them in a specific

context. Undoubtedly the capacity of the products to

induce intoxication would have attracted attention as

soon as they were discovered. Indeed we have ample

evidence that birds and mammals are attracted to

fermenting fruits, and will manifest clear evidence of

drunkenness, and even of addiction to ethanol. In

many cases the intoxication became associated with

religious experiences among humans. Despite these

complicating sociological factors, we can properly

see alcoholic fermentation as a preservation strategy,

essentially indistinguishable from those presented in

the preceding two sections. Sweet fruits have a very

short storage life, although strategies have been de-

veloped to permit storing some hard fruits (notably

apples and pears) for extended periods. At the other

extreme, grapes are so easily bruised that picking

them for table use demands great care; the yeasts

always present on the grape skins quickly ferment

the fruit juice at the slightest opportunity. The only

practical alternative to fermentation is drying to

raisins, currants, and sultanas.

0023 Roots, bulbs, and tubers In general, root crops are

stable enough for their storage in simple systems, and

even for them to be left in the ground during winter

until required. Thus, with minor exceptions such as

the radishes referred to above, root crops are not

fermented in temperate climates. Bulbs are also gen-

erally stable enough for winter storage, so fermenta-

tion in brine is probably done more for culinary than

for conservation reasons. The New World gave us,

among many other valuable crops, three novel

starchy crops that have now become so indispensable

that we often forget their origins. Of these, one is

a cereal (maize) but the other two are root crops,

potatoes (Solanum tuberosum), and cassava (Manioc

esculenta). Of these two, I have no knowledge of

potatoes being fermented, except in the very limited

sense of them being a source of starch for alcohol

production. Potatoes can produce various toxins as

defenses against predators, but protecting the tubers

from exposure to light easily prevents production of

the most important of these, and I am not aware of

any evidence that fermentations will reduce toxicity

of green tubers. On the other hand, fermentation is

absolutely essential for making cassava safe for use.

Most varieties are extremely toxic, because of the

presence of a cyanogenic glycoside. In the intact

tuber this, and the enzyme that can hydrolyze it, are

strictly segregated, but mechanical damage brings

them into contact, so releasing the highly toxic hydro-

gen cyanide. It is clear that even very primitive

peoples from its native habitats had developed tech-

niques for making the tuber comparatively safe to eat.

These are not primarily fermentations, depending as

they do on the enzymatic action described above to

destroy the cyanogenic glycoside. However, the con-

ditions under which the tubers are harvested and

prepared for detoxification insure that there is an

abundant microbial flora associated with them.

LAB, which do not use iron-containing enzymes, are

resistant to cyanide, and their growth on the cassava

portions produces acidic conditions that both favor

the action of the relevant enzyme and help in removal

of the cyanide as the unionized gaseous form. Subse-

quent processing includes drying, reduction to granu-

lar form, and heat treatments such as (in the case of

products such as the West Africa gari) roasting. Un-

fortunately, even garification will not reliably remove

the last traces of cyanide. Although the residual ma-

terial is below the acutely toxic concentration, it can,

by competing with iodide, produce the thyroid gland

malfunction known as goiter.

0024Seeds The plant products discussed so far have been

characterized by high water content. This it true even

of the firmest products, such as the root crops. This

water content means both that any injury leaves the

foodstuff liable to fermentation or other microbial

attack, and that even the undamaged item has a re-

stricted storage life because eventually water loss will

reduce it to a flaccid and uninviting state. However,

some vegetables can be made suitable for storage by

deliberate, controlled dehydration. With seeds, the

evolutionary development resulted in a very dry,

tough, long-lasting product. Seeds are also packed

with nutrients placed there by the parent plant to

support initial growth of the new plant whose embryo

the seed contains. Thus a seed has many characteris-

tics which make it potentially desirable as a human or

animal food. From the human viewpoint, however,

seeds have some disadvantages as foods. As har-

vested, they are difficult to eat. If processed in the

obvious way, by soaking and/or boiling in water, the

FERMENTED FOODS/Origins and Applications 2335

product is apt to be rather bland and unappetizing.

Indeed, of the various grains and seeds harvested by

humans, only rice is consumed in this way to any

extent. Commination by crushing or grinding can

effect limited improvements, but the resulting gruels

or porridges are still of limited appeal. Much the same

is true if the material is formed into a paste and baked

or roasted. On the other hand, even the simplest

fermentations can effect considerable improvements.

For example, a common breakfast dish in Africa is a

maize porridge in which the ground maize is left

overnight in water, and then boiled next morning,

ready for eating. Overnight there is substantial acid-

ification through the action of LAB. Although this is a

fairly minor change, the result is a much more appe-

tizing porridge, especially with the help of a little

crude sugar. Most such mixtures of flours and water

will develop substantial populations of LAB, alone or

associated with yeast cells. Microbial gas production

will cause some expansion of the paste or dough, and

give a tasty and appealing product upon cooking. The

most obvious example of this type is of course sour-

dough bread. It seems reasonable to believe that this

is a very ancient product, and archeological evidence

is emerging to support this view. A simple improve-

ment would be to add a part of a good ferment to a

fresh mixture of flour and water. This process, some-

times called ‘back slopping,’ remains the basis for

much sourdough bread production to the present.

0025 A more dilute mixture of flour and water would

give a crude alcoholic drink. The really important

development here was the discovery that germinating

the seeds greatly increased the alcoholic content, and

the general quality of the resulting drink. Beer pro-

duction in the west further modifies the properties of

the drink by drying and heat treatment of the germin-

ated seeds (barley malt). African sorghum beer does

not require this added refinement, and it seems rea-

sonable to think that the earliest barley fermentations

would have used ‘green’ (undried) malt. Again the

fermentations would have used a mixture of LAB

and yeasts. It is clear that from fairly early times

residual yeast from beer and wine fermentations was

used for bread making. Equally, kvass fermentation

from rye bread and water uses a portion of sourdough

bread ferment to start a new brew going, although

once started, it is maintained by ‘feeding’ the ferment

with additions of bread and water.

0026 Rice flour mixed with legume seed flour and water

will ferment with leavening provided by carbon diox-

ide generated by heterofermentative LAB. In parts of

India this simple process yields products such as idli

and dosa.

0027 Thus, seeds rich in starch are converted to many

foods and drinks by a range of fermentations which

depend on yeasts and LAB, alone or in associations.

Fermentations of protein-rich seeds, particularly the

soybean (Glycine max) and the ground nut (peanut,

monkey nut, Arachis hypogea), of tropical and sub-

tropical origin, together with the seeds of tropical

leguminous trees, have provided both staple foods

(such as tempeh and oncom (ontjom, onjom, etc.) )

and flavoring materials (soy sauce, miso, etc.)

throughout the tropics and subtropics for many thou-

sands of years. The driving force for such develop-

ments was probably the rather bland nature of the

starting materials, but we now know that fermenta-

tions can increase the digestibility of constituents of

the seeds, particularly the proteins, enrich the prod-

ucts with extra B-vitamins, decrease concentrations

of some toxic or antinutritional factors, and increase

the availability of essential mineral nutrients. These

fermentations are frequently multistage, using mold

fungi to manufacture a range of digestive enzymes,

then yeasts and LAB to complete the process. The

origins of these fermentations are lost in time, but

we know that soy sauce and miso have existed for at

least 3000 years. Legume seeds tend to be rather well

supplied with antinutritional factors, and detoxifica-

tion during the fermentation is a significant benefit of

the process. Perhaps the most remarkable example of

seed detoxification, however, concerns the castor

bean (Ricinus spp.). This seed contains a wealth of

toxic materials, including ricinoleic acid (a powerful

purgative), strongly allergenic proteins, and ricin.

Despite this, in parts of Nigeria the seeds are col-

lected, boiled, dehulled, wrapped in leaves, and

allowed to ferment, then used as a food flavoring,

apparently without any ill effects on its consumers.

Types of Fermentations

0028Although space constraints forbid a detailed discus-

sion, it is worth noting the range of fermentation

procedures developed for dealing with foods. The

simplest are probably the liquid fermentations used

in making drinks such as beers, wines, and some of

the milk products such as yogurt and buttermilk.

These are sometimes called suspension cultures be-

cause the microbial cells float suspended in the sur-

rounding liquid. Another name is stirred tank reactor

(STR) fermentations. Fermentations involving molds

usually require free access to the air, both to meet the

organism’s need for abundant oxygen, and to remove

the products of the fermentation, principally carbon

dioxide and heat. In one case however (tempeh) the

process requires a very limited exposure to oxygen,

traditionally achieved by wrapping the substrate in

banana or teak leaves, although plastic bags pierced

with a pattern of fine holes now often replace these.

2336 FERMENTED FOODS/Origins and Applications

Such fermentations, which do not require free liquid

water, are described as solid substrate fermentation

(SSF). Some lactic fermentations, for example of

starchy or farinaceous materials, might also be placed

here, as might sausage fermentations. When a solid

substrate is in free water, it appears that this is just a

type of suspension culture, but there is evidence to

suggest that the active microbes attach themselves to

the solid material to a considerable extent, thus pro-

ducing some characteristics of a SSF. The kefir grain

provides an interesting problem. Attachment of the

cells to the polysaccharide membrane suggests SSF,

but analysis of the fermentation shows that there are

large numbers of cells suspended in the liquid, quite

free of the grains, and that the proportions of bacter-

ial species in suspension are radically different from

the proportions within the grains. In Orleans vinegar

production the acetification is effected by a layer of

bacterial cells growing as a film or skin at the inter-

face between water and air, so exhibiting some char-

acteristics of a SSF. The ‘quick’ process features a

layer of cells on the surface of the wood shavings,

irrigated by the recycling liquid, but also supplied

with abundant oxygen, thus showing an even closer

relationship to SSF. Citric acid production by Asper-

gillus used to require static growth on the surface of a

liquid layer, rather like the Orleans vinegar process.

Some processes were described using growth on

bamboo supports and a liquid recycle like the

‘quick’ vinegar process, but it is not clear if these

were applied on a production scale.

The Future for Traditional Fermentations

0029 Some very ancient fermentations continue to flourish

and develop on a very large scale. Soy sauce produc-

tion almost seems capable of expansion without limit,

as does cheese. Yogurt has been a remarkable success

story, with market penetration far beyond its trad-

itional homelands. Vegetable fermentations, such as

sauerkraut and olives, also seem to grow, although

they perhaps do so more slowly than some of the

other cases cited. The sourdough bread story is an-

other remarkable one, with the product now on offer

at (it seems) every airport in the USA. There does not

seem to be any fear for the future of these and a

selection of other products.

0030 On the other hand, I feel substantial concern for

some of the more modest traditional fermentations

found in the developing countries. These have made a

significant contribution to the people’s nutrition in

the past, and the example of tempeh shows how

they can substantially improve the nutritional status

of the poorest folk. Tempeh itself seems to be robustly

addressing the challenge offered by modernizing

Indonesian society, but this is an exception. Sorghum

beer in South Africa is another example where (in this

case with intelligent support from central govern-

ment) a traditional food item continues to enjoy a

place in an evolving society’s markets. In many

cases, however, modernization tends to displace trad-

itional foods with imported ones perceived as more

‘western’ by precisely those consumers who are least

able to afford the change to imported food fashions.

The drift from rural to semiurban living exacerbates

the situation. The traditional food fermentations are

essentially rural, low-technology processes conducted

at an almost domestic level. Hygiene considerations

alarm the western observer, but in general the adapted

consumer population seems to suffer no harm from

these products. There are exceptions of course. The

continuation of poisoning outbreaks caused by con-

sumption of tempeh bonkrek in Indonesia, despite

the authorities’ efforts to ban its production, demon-

strate the kind of danger which exists. On balance,

however, I feel that loss of traditional knowledge

regarding the conduct and management of traditional

fermentations will be a serious matter. This know-

ledge tends to be the preserve of women. Young

people are not interested in learning about these

matters, and emerging societies tend to place an

even lower value on ‘women’s knowledge’ than de-

veloping ones do. Courses on food, and fermentation

need to place stress on the value of such information.

This is perhaps the only way in which we can hope to

conserve this unique knowledge pool.

See also: Bifidobacteria in Foods; Fermented Foods:

Origins and Applications; Fermented Meat Products;

Fermentations of the Far East; Beverages from Sorghum

and Millet; Soy (Soya) Sauce; Fermented Milks: Types of

Fermented Milks; Products from Northern Europe; Other

Relevant Products; Dietary Importance; Leavening

Agents; Mycotoxins: Classifications; Soy (Soya)

Beans: Processing for the Food Industry; Starter

Cultures; Yeasts