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sodium dodecyl sulfate–polyacryl amide gel electro-

phoresis) removed protein, glycerol, hexosamine,

sialic acid, and uronic acids from the crude slime

material. The phosphate group was attached to the

b-d-galactopyranosyl residue. The molecular weight

of this phosphopolysaccharide was estimated to be

1.7 10

by gel permeation chromatography. The

phosphopolysaccharide has a negative charge; it is,

therefore, possible that it could form complexes with

basic proteins found on the cell surface of lactococci,

due to electrostatic interactions.

Determinants of Glycocalyx Formation

0025 Plasmid DNA Observations of the loss of the

mucoidal (Mucþ) phenotype at higher incubation

temperatures led to studies which have demonstrated

the involvement of plasmid DNA in the synthesis of

glycocalyx by lactococci. The ropy phenotype of

strains of L. lactis ssp. cremoris was found to be

associated with a 17-MDa plasmid in Swedish strains

and with a 30-MDa plasmid in Finnish strains. This

indicates that distinctly different plasmids coding for

the ability to produce slime are present in separate

populations of starter bacteria. Plasmids on which

slime synthesis is encoded can be transferred to

strains with no slime-forming ability by a number of

currently available techniques, including electropor-

ation or cotransfer involving a bigger plasmid, on

which an ability to ferment lactose is encoded.

0026 Proteins of the cell surface Two cell surface proteins

of mol. wt 26 kDa and 42 kDa have been shown to be

associated with slime formation in lactococci. The

synthesis of these proteins is probably plasmid-

encoded.

0027Lipoteichoic acid Experiments demonstrating the

presence of lipoteichoic acid (LTA) antigen on

the cell surface of L. lactis ssp. cremoris led to a

hypothesis linking LTA with the formation of a

capsule or slime. LTA, which was also detected in

the growth medium during early stationary phase

and during storage at refrigeration temperature,

may form associations with proteins and polysacchar-

ides of the slime material. In addition, LTA present on

the cell surface inhibits autolytic enzymes of the bac-

terial cell wall, which has obvious advantages for

the shelf-life of the product. LTA also interferes with

cell division: 20% of the cells of one particular slime-

forming strain were found to have an abnormal

morphology due to disturbances in cell division

attributed to LTA.

0028Effect of limiting factors Even in the presence of an

energy source, bacterial growth may be affected by

some limiting factors, such as an unfavorable physical

or chemical environment or the exhaustion of an

essential nutrient. It has been suggested that the con-

tinuing catabolism of energy substrates can then pro-

vide an impetus for the production of polymers, such

as the slime material, as either energy reserves or

waste products.

0029Instability of slime production The variable rate at

which lactococci produce slime is a well-known phe-

nomenon, especially during incubation at a higher

temperature, e.g., 30



C. In addition, the serial

transfer of a ropy strain, even at a lower temperature

which normally favors the production of slime mater-

ial, often leads to the loss of this trait. Sometimes, this

unpredictability of slime formation causes difficulties

in the commercial manufacture of ropy fermented

milks.

0030Although the loss of the ropiness trait in starter

strains has been observed in the commercial produc-

tion of ropy milks, a similar problem has not been

reported in the traditional manufacture of these prod-

ucts, in which a mixture of undefined organisms is

used. A mixed population of lactococci and leuconos-

tocs is likely to have effective mechanisms for reten-

tion in the culture of the plasmid(s) on which the

ability to produce capsular material is encoded, espe-

cially if other properties important for the survival of

the bacterial population are encoded on the same

plasmid(s). The data reported in Table 1 lend support

to this concept.

tbl0002 Table 2 Composition of the slime material and phospho-

polysaccharide excreted by Lactococcus lactis ssp. cremoris SBT

0495

Content (%)

Crude slime

material

Purified

polysaccharide

Total carbohydrate 42.3 78.9

(90.5)

Rhamnose 21.7

Glucose 31.4

Galactose 38.0

Methylpentose 20.6 21.4

Hexosamine 4.8 ND

Sialic acid 0.8 ND

Uronic acid 1.9 ND

Glycerol ND

Phosphorus 1.8 3.1

Protein 21.2 ND

Values after hydrofluoric acid cleavage.

Not detected.

From Nakajima H, Toyoda S, Toba T et al. (1990) A novel

phosphopolysaccharide from slime-forming Lactococcus lactis subspecies

Cremoris SBT 0495. Journal of Dairy Science 73: 1472–1477 with permission.

2378 FERMENTED MILKS/Products from Northern Europe

Bacteriophage

0031 Attack by bacteriophages can cause problems in the

manufacture of ropy fermented milks. Thirteen

phages of different morphology have been found in

an extensive study on 90 samples of viili from 20

dairies in Finland. The main morphological type

was characterized by an isometric head with a long,

noncontractile tail. The host organisms for these

phages included strains of L. lactis sspp. cremoris

and Leuconostoc mesenteroides ssp. cremoris. Some

phages differed only in their host specificity.

0032 A phage of nonencapsulated L. lactis subsp. cre-

moris isolated from viili was shown to dissolve the

capsules of some strains, including a strain of L. lactis

ssp. lactis. The capsules disappeared soon after

infection, and maturing phages were seen inside the

cells 2 h after infection, appearing as tightly packed

bundles. The phage titer declined rapidly after

heating for 15 min at 50–70



C, but particles capable

of plaque formation were detected even after heating

for 5 min at 100



Products and Processes

0033 In the domestic production of fermented milks, no

heat treatment was applied to milk prior to fermenta-

tion, and the milk was inoculated with the residue

remaining in the fermentation vessel from the previ-

ous batch. In this way, a characteristic flora domin-

ated by lactococci became established in the vessel.

Nowadays, in the commercial production of Nordic

fermented milks, defined strains of starter micro-

organisms are used. The types of starter microorgan-

isms have a distinct influence on the properties and

shelf-life of these products.

0034 Scandinavian fermented milks fall into six major

classes, as shown in Table 3. Not all products in each

row are identical to each other; the table is provided

as a guide.

ngfil

0035La

ngfil or ta

tmjo

lk has a mild, sour taste and a ropy,

dough-like consistency produced by encapsulated

variants of lactococci. Occasionally, lactobacilli are

also found in this product. Traditionally, the leaves of

plants such as butterwort (Pinguicula vulgaris)and

sundew (Drosera species, especially Drosera rotundi-

folia) were added to milk before leaving it to sour.

They seem to exert a rennet-like action. No relation-

ship has been established between the bacterial flora

of butterwort or other plants and the bacterial com-

position of la

ngfil.

0036La

ngfil cultures were preserved for later use by

simple techniques, such as dipping a piece of cloth

(in Sweden) or birch twigs (tettemelk, in Norway) in

the finished product and then allowing them to dry. A

new batch was started by immersing the twigs, or

placing the dried cloth, in fresh milk.

0037Viili contains various lactose-fermenting yeasts and

Geotrichum candidum, in addition to lactococci and

leuconostocs. The cream layer is usually covered with

the mold. Viili is made from unhomogenized milk and

is eaten with a spoon.

0038Pitka

piima, which is always ropy, is used as a

drink. In domestic production, the cream layer, re-

moved from the pitka

piima after fermentation, was

used to make butter.

0039Viilipiima

, from which the cream is not removed,

also serves as a drink.

0040The following steps are included in the commercial

production of viili:

0041standardization of fat content at the minimum level

of 3.9%

0042heat treatment at 89–90



C for 15–30 min or 92–



C for 4–5 min

0043cooling to 18–20



0044addition of 4–8% starter culture

0045incubation for 18–20 h to reach the pH of 4.6

0046cooling to the storage temperature of 8–10



The final pH, after cooling, is 4.3–4.4 and the shelf-

life is between 10 and 15 days.

Cultured Milk

0047Filmjo

lk, sometimes also known as kulturmjo

lk (cul-

tured milk), is a popular Swedish fermented milk

characterized by a typical flavor and aroma (derived

primarily from diacetyl) and a fairly high viscosity,

with a fat content of 3.0%. Filmjo

lk, which is used as

a drink, was developed in the early 1930s. The starter

culture contains the acid-producer L. lactis ssp. lactis

and the flavor and aroma producers, L. lactis ssp.

lactis, L. lactis ssp. lactis biovar diacetylactis and

tbl0003 Table 3 The major classes of Scandinavian fermented milks

a,b

Sweden Norway Denmark Finland

ngfil Tettemelk Viili

Filmjo

lk Kulturmelk Tykmælk Talouspiim

Lttfil Skummet

Kulturmelk

Rasvatonpiim

Krnmjo

lk Kjernemelk Kærnemælk Kirnupiim

Grddfil Rømme Cre

me fraı

che Kermapiim

Lactofil Ymer Kokkeli

Each row represents a separate class of products.

There are also many special product names used by commercial

manufacturers of fermented milks.

FERMENTED MILKS/Products from Northern Europe 2379

Leuconostoc mesenteroides ssp. cremoris. All these

strains are propagated together.

0048 In the production of filmjo

lk:

0049 standardized milk is often deaerated at 78



Cto

prevent or to alleviate defects such as syneresis of

the coagulum, granulation, lumpiness, and low

viscosity

0050 the deaerated milk is homogenized at 10–20 MPa

and 70



C, and then heated at 95



C for 2–6 min

0051 the milk is cooled to 17–24



C and inoculated with

1% starter culture

0052 after 17–24 h, coagulum forms at pH 4.6

0053 the product is cooled to 8



C and packaged into

retail containers.

Normally, a shelf-life of 10 days at 8



C is achieved.

0054 Filmjo

lk with 0.5% fat is called la

ttfil; the same

product is known as skummet kulturmelk in Norway.

0055 Tykmælk, a characteristic Danish fermented milk,

is produced commercially in a similar manner to the

Swedish filmjo

lk. It contains 3.5% fat.

Buttermilk

0056 Traditional buttermilk (ka

rnmjo

lk, kjernemelk, kær-

nemælk, kirnupiima

) is made by churning cultured

cream which has a relatively low fat content. In this

manner, a small amount of cultured butter and a

relatively high volume of buttermilk are obtained. A

product known as cultured buttermilk is made by the

fermentation of skim milk or low-fat milk.

0057 Starter cultures contain, in addition to the bacteria

used for filmjo

lk manufacture, Lactococcus lactis ssp.

cremoris. Slime-producing strains are included in the

starter culture for some types of cultured buttermilk

made in Finland. The production process involves:

0058 heat treatment at 85–90



C/20–30 min or 92–



C/4–5 min

0059 cooling to 20–23



0060 incubation with 1–4% starter culture

0061 15–20 h fermentation

0062 cooling to 5–10



C, during which the pH decreases

to 4.4–4.45.

The flavor and aroma of cultured buttermilk are very

similar to those of filmjo

lk. The shelf-life varies from

7 to 12 days.

Cultured Creams

0063 Gra

ddfil, rømme, cre

me fraı

che and kermapiima

are

cultured creams made by the fermentation of heat-

treated cream with the same cultures that are used in

the manufacture of cultured buttermilk. The legal

requirements regarding the fat content of cultured

creams and production practices vary between Scan-

dinavian countries. For example, in Denmark, pro-

duction involves:

0064the cream being standardized at 9, 18, 38 or 50%

fat, and then homogenized

0065heat treatment at 90



C for 5 min

0066cooling to the incubation temperature of 20–27



0067inoculation with 2% starter culture

006816–20 h incubation in the tank

0069cooling to 5



C, during which the pH of the final

product falls to 4.4.

In two types of Swedish gra

ddfil, the legally required

fat content is 12 and 34.5%; Norwegian rømme con-

tains 20 or 35% fat; and in Finland there are three

types of cultured cream, at >12, 35–40 and 42% fat.

Concentrated Fermented Milks

0070These include ymer, lactofil, kokkeli, and skyr.

0071Ymer is a Danish fermented milk, which contains

at least 11% nonfat milk solids (including 5–6%

protein) and 3.5% fat. It is usually produced from

the ultrafiltered retentate, which contains about 15%

total solids. Production involves:

0072blending retentate with cream and homogenization

0073heat treatment at 90



C for 5 min and cooling to

20–27



0074inoculation with 4% starter culture containing L.

lactis sspp. lactis and cremoris and Leuconostoc

mesenteroides ssp. cremoris

0075fermentation until the pH reaches 4.5 (after 16–

20 h)

0076stirring, cooling to 5



C, and storage for 24 h

0077stirring again and packaging.

The product is often cooled in two stages, first to



C and then to 5



0078In the traditional process, fermentation of the skim

milk is followed by cutting of the coagulum and

drainage of the whey at 40



C. Alternatively, a quarg

separator can be used to remove the whey. Pasteur-

ized cream is then blended with the skim product, and

this is followed by homogenization, cooling to 12–



C and packaging. The shelf-life of ymer is 20

days at 5



0079Lactofil, produced in Sweden, is similar to ymer.

The fat content in lactofil is 5% and the starter cul-

ture is similar to those used in the manufacture of

filmjo

lk and karnmjo

lk.

0080Kokkeli, traditionally made in eastern Finland, is

prepared by warming spontaneously soured milk in

an oven and removing the separated whey.

0081Skyr is manufactured in Iceland from skim milk.

Unlike all other traditional Scandinavian fermented

2380 FERMENTED MILKS/Products from Northern Europe

milks, it is fermented by a thermophilic microflora.

The milk is then heated to facilitate the syneresis of

the protein coagulum. Whey separation is achieved

by either straining through linen bags or using quarg

separators. Ultrafiltration is now also used to recover

whey proteins, which are added to the skyr before

packaging. Microorganisms isolated from skyr in-

clude thermophilic lactic acid bacteria (Streptococcus

thermophilus, Lactobacillus delbrueckii ssp. bulgari-

cus and L. helveticus) and lactose-fermenting yeasts.

Typical skyr contains 17.5% total solids, including

>13% protein and 0.4% fat.

Product Composition and Shelf-life

Composition

0082 The total solids and fat content of Nordic fermented

milks is prescribed by law. Often, a minimum number

of viable microorganisms is prescribed by the food

standards.

0083 Starter activity in milk leads to the production of

lactic acid, as well as flavor and aroma compounds.

For example, Lactococcus lactis ssp. lactis metabol-

izes the citrate present in milk to diacetyl, acetoin,

2,3-butylene glycol, and CO

. Citrate is also metab-

olized by leuconostocs, mainly to diacetyl and acetoin

(at pH 5.5), and acetate (at pH > 5.5).

0084 Differences in vitamin content have been observed

between fermented milks and raw milk. For example,

viili and cultured buttermilk (containing 1.9% fat)

were found to contain more folate than raw milk,

by 48 and 65%, respectively. However, their vitamin

C content was lower than that of milk, by 58 and

24%, respectively, and their riboflavin was lower, by

12 and 11%, respectively. The concentration of

vitamin B

in both products was also lower than

in milk, by > 20 %.

Shelf-life

0085 Very high numbers of viable bacteria have been

observed in some spontaneously fermented milks.

This may be due to the reduced rate of cell autolysis

(discussed above).

0086 The shelf-life of traditional ropy fermented milks is

exceptionally long, due mainly to the presence of

glycocalyx, which improves the rheological behavior

of these products.

0087 Features such as the cream layer and the presence

of the mold Geotrichum candidum on the surface of

some products provide added protection from spoil-

age organisms, thus further extending the shelf-life.

0088 Commercially made products are also noted for

their long shelf-life. Even if some preexisting defect

reduces the water-holding capacity of the protein

matrix, e.g., if proteolysis were allowed to proceed

unhindered in raw milk, the presence of glycocalyx

would mask the syneresis of the protein coagulum.

Health-related Effects

0089Considerable progress has been made in demonstrat-

ing certain beneficial effects of Nordic fermented

milks in experimental animals. However, unequivocal

experimental and/or epidemiological evidence still

needs to be gathered to substantiate claims of similar

effects in humans.

Effect on Immunity

0090It has been suggested that fermented milks may play

an immunomodulating role, for example they stimu-

late the functions of gut-associated lymphoreticular

tissue (GALT), and this effect has been attributed

mainly to antigenic structures of the surface of lacto-

cocci. In particular, L. lactis ssp. cremoris isolated

from viili has been shown, in studies with human

lymphocyte cultures, to stimulate the secretion of

immunoglobulins, primarily those of the immuno-

globulin M class. In addition, T lymphocytes showed

considerable proliferation in response to the same

strain.

0091A substance active as a mitogen of murine B cells

was purified from the slime produced by another

strain of L. lactis ssp. cremoris, also isolated from

viili. The mitogenic compound was a phosphopoly-

saccharide, containing rhamnose, glucose, galactose,

and phosphorus. Its activity was higher than that of

unpurified slime.

0092A significant induction of the cytotoxicity of

peritoneal murine macrophages against sarcoma

cells, by L. lactis subsp. cremoris isolated from viili,

has been demonstrated in vivo. A single intraperi-

toneal injection of the freeze-dried cells retarded

the growth of ascitic and solid sarcomas in mice.

However, the same preparation showed no direct

cytotoxic activity against the same sarcoma cells

in vitro, which suggests that the antitumor effect of

this organism is through the enhancement of the

cytotoxicity of the macrophages of the host. The

exact mechanism of this enhancement is not known,

but the slime has been observed to increase glucose

consumption in vitro by intraperitoneal macro-

phages.

0093Freeze-dried preparations of viili, la

ngfil, and ropy

yogurt, used as intraperitoneal injections daily for 9

days after the tumor inoculation, also significantly

retarded the growth of murine solid sarcomas

in vivo. The maximum antitumor effect was induced

by a dose of 10 mg kg

1

of the viili preparation,

50 mg kg

1

of the la

ngfil preparation and 100 mg

FERMENTED MILKS/Products from Northern Europe 2381

1

of the ropy yogurt preparation. Thus, the effect

of both viili and la

ngfil was clearly stronger than that

of ropy yogurt. All three preparations significantly

enhanced the delayed cutaneous hypersensitivity re-

sponse to oxazolone, which was depressed in tumor-

bearing mice. The antitumor effect of these ropy

milks is thought to be mediated by the immune

responses associated with host’s macrophages and/or

T cells.

Antimutagenic Activity

0094 Strains of L. lactis ssp. cremoris isolated from viili,

both ropy and nonropy, reduced the mutagenicity of

nitrosated beef extract by 40%, as determined by the

Ames test, using Salmonella typhimurium as the test

organism.

Lowering of Serum Cholesterol

0095 In experiments on rats receiving diets containing

viili, nonropy fermented milk, or acidified skim

milk, the serum cholesterol level of rats on a viili-

containing diet was lowest of the three groups.

Their ratio of high-density lipoprotein cholesterol to

total cholesterol was the highest of the three groups.

The mechanism of this cholesterol-lowering effect is

unknown.

Antibacterial Effects

0096 Antagonistic effects of lactic acid bacteria against

common pathogens and spoilage bacteria have been

well demonstrated in vitro. For example, lactococci

and their capsular material have been shown to in-

hibit the growth of Staphylococcus aureus, Escheri-

chia coli, and some clostridia.

Future Trends

0097 The future position of Nordic fermented milks in

their traditional markets seems assured, despite the

popularity that yogurt and probiotic products have

gained in the past few decades.

0098 Many types of fermented milks are produced now-

adays in Scandinavia and some of them do not clearly

fit into the categories outlined above, for example,

products which are mixtures of ropy milks with

acidophilus milk. With the growing interest in

various probiotic cultures, this trend is expected to

continue, with more combinations of this kind being

offered to consumers.

See also: Cream: Types of Cream; Fermented Milks:

Types of Fermented Milks; Lactic Acid Bacteria;

Mycotoxins: Classifications; Probiotics; Starter

Cultures; Yeasts

Further Reading

Alm L and Larsson I (1983) Fra

n forntid till framtid. Den

nordiska ta

tmjo

lken – en produkt med gamla anor.

Nordisk Mejeriindustri 10: 396–399.

Bertelsen E (1983) Kulturmjo

lksprodukter i Norden. Nor-

disk Mejeriindustri 10: 386–390.

Forse

n R (1966) Die Langmilch (Pitka

piima

). Meijeritieteel-

linen Aikakauskirja 26: 1–76.

Forse

n R (1989) Characterisation of antigenic surface struc-

tures of lactococci and their possible immunobiological

effects. In: Fermented Milks and Health, workshop pro-

ceedings, Arnhem, September 1989. Ede, The Nether-

lands: NIZO.

Forse

n R, Niskasaari K, Tasanen L and Nurmiaho-Lassila

E-L (1989) Studies on slimy lactic acid fermentation:

detection of lipoteichoic acid containing membrane

antigens of Lactococcus lactis ssp. cremoris strains by

crossed immunoelectrophoresis. Netherlands Milk and

Dairy Journal 43: 383–393.

Gudmundsson B (1987) Skyr. Scandinavian Dairy Industry

4: 240–242.

IDF (1988) Fermented milks – science and technology.

International Dairy Federation Bulletin no. 227, 164 pp.

Kitazawa H, Toba T, Itoh T, Kumano N and Adachi S

(1990) Antitumor activity of ropy sour milks in murine

solid tumor. Japanese Journal of Zootechnical Science

61: 1033–1039.

Kitazawa H, Itoh T and Yamaguchi T (1991) Induction of

macrophage cytotoxicity by slime products produced by

encapsulated Lactococcus lactis ssp. cremoris. Animal

Science and Technology 62: 861–866.

Kitazawa H, Toba T, Itoh T, Kumano N, Adachi ST and

Yamaguchi T (1991) Antitumoral activity of slime-

forming, encapsulated Lactococcus lactis ssp. cremoris

isolated from Scandinavian ropy sour milk, ‘‘viili’’.

Animal Science and Technology 62: 277–283.

Kitazawa H, Yamaguchi T, Miura M, Saito T and Itoh T

(1993) B-cell mitogen produced by slime-forming,

encapsulated Lactococcus lactis ssp. cremoris isolated

from ropy sour milk, viili. Journal of Dairy Science 76:

1514–1519.

Kontusaari S and Forse

n R (1989) Finnish fermented milk

‘‘viili’’: involvement of two cell surface proteins in pro-

duction of slime by Streptococus lactis ssp. cremoris.

Journal of Dairy Science 71: 3197–3202.

Laukkanen M, Antila P and Antila V (1988) The water-

soluble vitamin contents of Finnish liquid milk products.

Meijeritieteellinen Aikakauskirja 46: 7–24.

Macura D and Townsley PM (1984) Scandinavian ropy

milk – identification and characterization of endogenous

ropy lactic streptococci and their extracellular excretion.

Journal of Dairy Science 67: 735–744.

Nakajima H (1995) Characteristics of fermented milk

produced by slime-forming Lactococcus lactis subsp.

cremoris. Snow Brand R&D Reports 104: 97–169.

Nakajima H, Toyoda S, Toba T et al. (1990) A novel phos-

phopolysaccharide from slime-forming Lactococcus

lactis subspecies cremoris SBT 0495. Journal of Dairy

Science 73: 1472–1477.

2382 FERMENTED MILKS/Products from Northern Europe

Neve H, Geis A and Teuber M (1988) Plasmid-encoded

functions of ropy lactic acid streptococcal strains from

Scandinavian fermented milk. Biochimie 70: 437–442.

Robinson RK and Tamime AY (1990) Microbiology of

fermented milks. In: Robinson RK (ed.) Dairy Micro-

biology, vol. 2: The Microbiology of Milk Products, 2nd

edition, pp. 291–343. London: Elsevier Applied Science.

Saxelin M-L, Nurmiaho-Lassila E-L, Merilainen VT and

Forse

n R (1986) Ultrastructure and host specificity of

bacteriophages of Streptococcus cremoris, Streptococcus

lactis subsp. diacetylactis, and Leuconostoc cremoris

from Finnish fermented milk ‘‘viili’’. Applied and Envir-

onmental Microbiology 52: 771–777.

Sundman V (1953) On the microbiology of Finnish ropy

sour milk. Proceedings of the Thirteenth International

Dairy Congress, vol. 3, pp. 1420–1427. The Hague, The

Netherlands: Mouton & Co.

Other Relevant Products

B McKevith and C Shortt, Yakult UK Ltd, Acton,

London, UK

Introduction

0001 Fermented milks and other related products are

available in many different countries worldwide.

Some have a long history of consumption while

others have been developed more recently due

to scientific advances. The microorganisms used to

make these products are varied but often feature

lactic acid bacteria (LAB) which during fermentation

convert lactose into lactic acid. Many of these prod-

ucts are generally good sources of a number of im-

portant nutrients such as protein, calcium, and zinc

and some also have other beneficial effects (particu-

larly on the gastrointestinal tract (GIT)). Indeed, in

some parts of the world these products have a long

history of therapeutic use. Due to increased medical

interest early in the twentieth century, many products

were developed commercially. Currently one of the

major areas for growth is the development of

fermented products containing specific probiotic

bacteria.

History

0002 The true origin of fermented milks is difficult to

establish but it is suggested that they originated

in western Asia and were carried to the east where

new variants were developed to suit the different

climate. Recipes for soured milks containing fruits

and spices existed in ancient Greek and Roman

times and fermented milks have played a role in

many different cultures throughout history, e.g.,

they are mentioned in the Bible and the sacred

books of Hinduism. Storable dairy products, pre-

sumably cultured, are also mentioned in the

archaic texts from Mesopotamia dating back to

before 3000 bc. In the preindustrial world, milk

and/or dairy products of some description had a

place in the diet of most people who had domesti-

cated animals. A combination of chance contamin-

ation, climatic conditions, and serendipity probably

played a part in the development of traditional

fermented dairy products. Fermentation of milk

allowed humans to store and use excess milk and to

travel long distances. Today, fermentation is used to

produce dairy foods with different flavors, textures

and health benefits.

0003Several different factors influence the preparation

of traditional fermented milk products, with agricul-

tural factors heavily affecting the process (Table 1).

Cultured dairy products can be prepared from the

milk of different mammals, with cows’, buffalos’,

goats’ and sheep’s milk being the most common. In

some parts of the world the milk of other animals

(such as camel, yak, and reindeer) is used.

0004Yogurt and fermented milk of some description are

probably the most popular fermented dairy products.

Variations within countries and even within regions

are seen due, in part, to different ethnic groups with

distinct cultures and preferences. Some of the trad-

itional fermented milks and related products pro-

duced in different parts of the world are outlined in

Table 2.

tbl0001Table 1 Factors influencing production of traditional fermented

milk products

Factor Example

Agricultural Current farm practices

Animal husbandry

Milk availability

Species of animals used for milk production

Species of animals used for other

agricultural purposes

Breed of species for milk production

Consumption and suitability of milk

Environmental Weather patterns

Climate

Cultural Eating habits of population

Stage of development of

commercial milk processing

Consumption and suitability of milk

Adapted from FAO (1990) Animal Production and Health Paper. The

Technology of Traditional Milk Products in Developing Countries. Rome: FAO/

WHO.

FERMENTED MILKS/Other Relevant Products 2383

Fermented Milks and Other Related

Products – Definitions

0005 Generally, fermented or cultured dairy products are

made from milk (or its components) and modified by

incubation with cultures of microorganisms. The

1997 International Dairy Federation (IDF) inter-

national draft standard described fermented milks as

milk products fermented by the action of specific

microorganisms and resulting in a reduction of pH

and coagulation. The microorganisms must ‘be

viable, active and abundant (at least 10

CFU g

1

)in

the product to the date of minimum durability.’ The

standard further controls the type of microorganisms

to be used as being nonpathogenic and nontoxic to

produce either a pure fermentation (a lactic acid fer-

mentation) or a mixed fermentation (containing also

an alcoholic fermentation). Specific cultures are re-

quired to be used for the production of certain defined

products, such as cultured buttermilk, yogurt, and

Acidophilus milk. There is some disparity among

different countries regarding the legal definition of

some fermented milk products. Some countries have

prescriptive legislation, in line with the above IDF

standard, while many others do not.

0006Some definitions for fermented milks and/or re-

lated products imply or state (in legislation or indus-

try standards) that live microorganisms should be

present in the final product. This is true in countries

such as Japan, the Netherlands, Denmark, and Aus-

tria, which stipulate that there must be a high propor-

tion of viable microorganisms in the product (often

10

1

). In contrast, a few countries such as the

UK, Germany, and Sweden also recognize products

that are heat-treated after fermentation as long as the

appropriate consumer labeling is used.

0007Currently changes are being proposed by the

Codex Committee on Milk and Milk Products to

the standard for fermented milks. The forthcoming

standard will cover all fermented milks (including

yogurt and composite products), give descriptions of

the different products, essential composition and

quality factors, food additives, contaminants, hy-

giene, and labeling. Issues currently under discussion

include at what point the viable organisms should be

controlled (e.g., at point of sale to the consumer,

when the product leaves the manufacturer, or at the

date of minimum durability); the definition, compos-

ition, and minimum acidity for mild yogurt; the def-

inition of composite fermented milk products, and

the labeling of heat-treated products. The standard

still has several hurdles to overcome before it is

adopted.

0008Below are some descriptions for fermented prod-

ucts that are currently used.

Yogurts

0009Yogurt is traditionally produced from milk and/or

cream through the action of two particular strains

of LAB – Lactobacillus bulgaricus and Streptococcus

thermophilus. Codex currently defines yogurt as a

milk product obtained by fermentation using these

two specific strains with or without optional add-

itions (such as milk powder, other LAB, and sugar).

In many countries (e.g., Sweden, France, Belgium,

Portugal, Spain, USA) legislation exists allowing

only L. bulgaricus and S. thermophilus to be used to

produce yogurt. In the UK yogurt can be made using

both of these strains or just one of them. In other

countries (e.g., Switzerland) strains such as L. acid-

ophilus and bifidobacteria may be used in addition

to the traditional yogurt strains. It is likely that the

tbl0002 Table 2 Examples of traditional fermented milk products and

other related products

Regions Products

Eastern Europe

Bulgaria Kisle mliako, Bulgarian milk, brano

mliako, boza

Czech Republic Kefir, Acidophilus sour milk, biokys

Hungary Sour cream, yogurt (tarho)

Poland Kefir, buttermilk, milk ‘‘champagne,’’

polkrem (soured cream)

Romania Oxygala

Middle and Near East

Greece Tiaourti

Israel Leben, zivda

Iran Dough, Kashk

Iraq Leben, kushuk

Lebanon Laban

Turkey Ayran, torba

Syria Lebnye, lebenen bezet

Africa

Algeria Aoules, tammart

Egypt Bouza, laban zabady, laban

rayeb, laban khad

Kenya Maziwa iala, busaa

Nigeria Nono

South Africa Magou, maas

Sudan Goubasha

Russia Kefir, koumiss, prostokvasha, rjazhenka

Scandinavia

Denmark Tymaelk ymer

Finland Piima, kurz, villia

Iceland Skyr

Norway Taette (cellar milk), seterroømme

Sweden Ropy milk

Asia

China Targ, airak

India Dahi, lassi

Mongolia Koumiss, tarag

Adapted from IDF (1988) Fermented milks and science and technology.

Bulletin of the International Dairy Federation 227: 4–164 and Kurman JA,

Rasic

JLJ and Kroger M (1992) Encyclopedia of Fermented Fresh Milk

Products. New York: Van Nostrand Reinhold.

2384 FERMENTED MILKS/Other Relevant Products

new Codex standard will build on the draft definition

currently used for mild yogurt (a product made

from S. thermophilus and lactobacilli other than

L. bulgaricus). In Japan no separate legislation exists

for yogurt and so it is not obligatory that the two

traditional strains are used, either collectively or

separately. Similarly, in Finland there are also no

compositional regulations for any milk products.

Soft Cheeses

0010 Cottage cheese is a high-moisture, unripened soft

cheese made from skimmed milk. Most of the

microorganisms used in its manufacture (including

species of Lactococcus lactis) are destroyed during

the process, which involves scalding the curds. After

washing, the curds are then mixed with a creamy

dressing, which has usually been ripened with a

flavor-producing culture. Cream cheese is a soft

cheese that is made from cream. A starter culture of

S. lactis and two species of L. lactis is used to produce

a rich, full, and mildly acidic flavor and a soft texture.

Cream cheese can be made from cream of various fat

contents. Cre

me fraı

che is a lightly fermented cream

with a rich nutty flavor. Cultured or sour cream is also

prepared from cream. After pasteurization and hom-

ogenization, it is incubated with a mesophilic starter

to produce a thick tangy product. Fromage frais is

made from fermented milk and has a mild flavor. It

is thicker and more concentrated than yogurt as some

water is removed after fermentation. Quark or quarg

is a soft, unripened cheese made in a similar way to

cottage cheese. Its production often involves heating

after coagulation by the starter culture.

Probiotic-Type Products

0011 Probiotic products contain live microbial food ingre-

dients that are beneficial to health. Bacteria of human

origin are often used in probiotic products intended

for humans. Species of lactobacilli and bifidobacteria

are most common but bacteria of nonhuman origin

and yeasts such as Saccharomyces boulardii are also

used. In some countries Streptococcus thermophilus

and L. bulgaricus are considered probiotic strains.

Fermented milk drinks and yogurts are popular

forms for probiotic foods, although nondairy fer-

mented products also exist, such as fruit juice drinks.

Other Fermented Drinks

0012 The proposed Codex standard will characterize cer-

tain fermented milks, including Acidophilus milk,

kefir, and kumys, by their specific microorganism(s).

However there are a number of other products

which are described elsewhere. Acidophilus milk is a

product made using the probiotic bacteria L. acid-

ophilus, a bacterium from the flora of the normal

GIT. It and related products (such as Acidophilus

yogurts) are popular in the USA.

0013Cultured buttermilk was originally made using

buttermilk (the byproduct of churning fermented

cream into butter) but it has an unpredictable

quality and short shelf-life since the whey often sep-

arates out and off-flavors develop. Modern equiva-

lents are made from skim or low-fat milk and

fermented with acid and flavor starters such as

S. lactis and/or S. cremoris together with S. paracitro-

vorous. Buttermilk is often used as an ingredient in

the baking industry.

0014Laban is a cultured milk drink, usually based on

cows’ milk and consumed in many Gulf countries.

Similar products exist in Egypt, Tunisia, and Mo-

rocco. Homemade traditional laban contains a mix-

ture of LAB, molds, and yeasts. Three strains of LAB

are used in its commercial preparation. Lassi is a

yogurt drink from East India that may be sweetened

and flavored with rosewater or fruit. Kefir originated

in Russia and is now also popular in Poland, Ger-

many, and Sweden. This traditional product is usually

made using cows’ or goats’ milk and kefir grains

which contain a complex mixture of microorganisms

including bacteria (such as streptococci and lactoba-

cilli), yeasts, and a polysaccharide of microbial origin.

Koumiss (kumiss, kumys, kumyss) also originated in

Russia but is based on mares’ milk. L. bulgaricus and

lactose-fermenting yeasts are used in its production.

Ropy milks, popular in Scandinavia, use starters that

produce slime (mucus), giving a unique viscous

quality to the final product.

Frozen Products

0015There are a few frozen products, like tsutsugi from

Mongolia, made from naturally fermented cream,

and a number of newer products like Acidophilus

icecream in the USA, which contain probiotic strains.

Although viability may decrease slightly during

freezing, it is still possible to achieve levels of 10

–

CFU ml

1

in frozen products. Frozen yogurt has

become popular since the 1970s, especially in the

USA. It is made by freezing regular stirred yogurt

after the addition of stabilizers, sweeteners, and fruit

and flavorings.

Other Related Products

0016Some fermented products are made using non-

dairy ingredients such as soya milk, coconut milk,

grains, and rice as a base, e.g., boza, a nonalcoholic

drink made from cereal (such as wheat, rye, maize, or

millet) and widely consumed in Bulgaria and the

Balkan peninsula. Acidified milk products (such as

sour cream) can be made by direct acidification using

organic acids. Nonfermented products also exist,

FERMENTED MILKS/Other Relevant Products 2385

such as nonfermented Acidophilus milk, available in

the USA where L. acidophilus is added to freshly

pasteurized milk and the product is then kept refriger-

ated to prevent bacterial growth. In this way the milk

acts as a carrier for the microorganism but it does not

have the sour taste usually associated with fermented

dairy products.

Microbiology

0017 Originally the microorganisms involved in fermenta-

tion were used to preserve food of animal and plant

origins. As other methods are now available (e.g.,

refrigeration and pasteurization), microorganisms

are used for other reasons – to change the flavor of

the raw material (possibly to produce a more accept-

able product), to improve the nutritional value of the

raw material, and to produce a food which offers

beneficial health effects (e.g., probiotic products).

0018 The microorganisms used in the starter culture

determine the characteristics of the final product.

More specifically, the product’s quality and charac-

teristics are dependent on the way the chosen micro-

organisms utilize the nutrients available in the

medium.

0019 Historically, fermented dairy products were made

using starter cultures containing a heterogeneous

mixture of LAB and yeasts, using one batch to inocu-

late a subsequent one. This wild fermentation can

lead to products of variable quality and taste, due to

contamination and the genetic instability of some

microorganisms. Although this traditional method is

still used in many parts of the world (especially for

home production), starter cultures containing known

microorganisms have been available commercially

since the beginning of the twentieth century. The

starter cultures act in a known way, giving greater

control over the end product in terms of safety, qual-

ity, and taste.

0020 Specific starter cultures are often used in geograph-

ical regions, for example, ropy, sour milks containing

only streptococci or streptococci and lactobacilli

predominate in northern Europe. The type of starter

culture can be used to classify fermented milk

products in the following manner (Table 3).

0021 LAB are Gram-positive nonsporing cocci, cocco-

bacilli, or rods. Lactobacilli are generally recognized

as safe because of their extensive use over the centur-

ies and more recently their role in food technology,

with negligible problems. LAB involved in the pro-

duction of fermented milks and related products are

distributed over a large number of bacterial species

and include species of Lactobacillus, Streptococcus,

and Bifidobacteria genera. Lactobacilli have greater

difficulty growing in milk that is neutral or slightly

alkaline compared to streptococci. In a mixed culture

of these two species, the streptococci may establish

growth in neutral or weakly alkaline milk, and from

their acid production make the milk suitable for

subsequent lactobacilli growth.

0022LAB use the lactose in milk as an energy source.

During fermentation lactose is cleaved by bacterial

enzymes to produce galactose and glucose. The glu-

cose formed is then further fermented to produce

pyruvic acid, which is metabolized to lactic acid.

There are no traditional products made solely using

yeast but some products such as kefir and koumiss

use yeasts as well as LAB in their manufacture. The

yeasts produce CO

via an alcoholic fermentation.

This CO

may be utilized by the other microorgan-

isms and therefore is not usually present in the final

product.

0023Many products have been developed over the last

100 years due to advancements in microbiology,

increased understanding of the fermentation pro-

cess, and increased knowledge of the impact of nutri-

tion on health. Unlike products which often rely on

spontaneous fermentation, newer products use

selected strains of bacteria for specific qualities.

Some commercialized products may be copies of

traditional products, for example, using different

microorganisms to produce a product similar to a

traditional one.

tbl0003Table 3 Classification of fermented milk products by starter

culture

Starter culture used Example of fermented dairy

product

Thermophilic

Classic cultures, e.g.,

Lactobacillus bulgaricus and

Streptococcus thermophilus

Yogurt

Acid buttermilk

Mesophilic

Some species of streptococci,

e.g., Streptococcus lactis,

lactococci and some

Leuconostoc species

Conventional buttermilk

Cream cheese

Cre

me fraı

che

Cottage cheese

Fromage frais

Sour cream

Ropy milks – Scandinavia

Lactic acid bacteria/yeast

Mixture of lactic acid bacteria and

yeasts, e.g., Saccharomyces

lactis

Kefir

Koumiss

Probiotic

Some species of lactobacilli, e.g.,

Lactobacillus acidophilus, L.

casei, and bifidobacteria, e.g.,

Bifidobacteria bifidum

Bioyogurts

Acidophilus milk

Yakult

Adapted from National Dairy Council (1997) Topical Update 8. Nutritional

Benefits of Yogurt and Other Fermented Milk Products and IDF (1988)

Fermented milks and science and technology. Bulletin of IDF 227: 4–164.

2386 FERMENTED MILKS/Other Relevant Products

Probiotics

0024 Most microorganisms in fermented milks and related

products do not survive transit through the GIT. The

body has a number of different mechanisms (e.g.,

stomach acid, bile, and mucous secretions of the

GIT) to decrease or prevent the movement of micro-

organisms through the GIT. Only robust strains (usu-

ally of human origin) such as those termed probiotics

can survive and reach the large intestine in a viable

state. Here they can modulate the gut flora, leading to

specific health benefits.

0025 The word probiotic is derived from the Greek,

meaning for life. The concept was used by von Ferdi-

nand in 1954 to describe gut flora modulation using

lactobacilli and bifidobacteria. The definition has

evolved and recently probiotics for use in human

nutrition were redefined as ‘live microbial food

ingredients that are beneficial to health.’ As such a

probiotic may consist of a single strain or mixture of

microorganisms, its activity is not limited to the GIT

but may affect microbial communities at other sites,

such as the urogenitial and respiratory tracts; it may

have nonmicroflora-mediated effects, e.g., effects on

immune parameters.

0026 A number of microorganisms are used in probiotic

products, including strains of lactobacilli (e.g.,

L. acidophilus, L. casei,andL. plantarum), bifido-

bacteria (B. breve, B. longum, and B. bifidum), other

LAB (e.g., Enterococcus faecium) and non-LAB

species such as strains of Escherichia coli.

0027 Although viability has been stressed as an import-

ant criterion for probiotic microorganisms, recent

studies have shown that nonviable probiotic organ-

isms and their cellular components may be efficacious

in certain situations. Research in this area is ongoing

but, from a commercial perspective, viability of the

microorganisms in probiotic products continues to be

a key issue.

Nutritional Aspects

0028 Fermented milks and related products reflect the

nutritional composition of the milk or base ingredi-

ent from which they are made. Generally those made

from milk are good sources of a wide variety of

nutrients but their nutritional composition often

varies from milk due to changes during fermentation

(Table 4).

0029 Cultured products are more digestible compared to

unfermented ones. In some communities fermented

products are used as weaning foods for this reason.

During fermentation acid is produced slowly,

allowing small particles to form and increasing the

surface area for later human enzyme digestion.

0030Fermented milk products have lower lactose

levels than milk, normally ranging from 30 to 50%.

This is because lactose is hydrolyzed by microbial

beta-galactosidase during fermentation to produce

galactose and glucose, making fermented products

useful for the substantial number of people with a

lactase deficiency (absence or decreased production

of the enzyme needed to break down lactose).

Also live bacteria from fermented products that

survive the gastric acid release their microbial beta-

galactosidase into the small intestine, aiding lactose

digestion.

0031A larger proportion of free amino acids and pep-

tides will be present in fermented milk products due

to microbial digestion, although the overall amino

acid concentration will be similar to the base ingredi-

ents. This may not be of major importance, as most

people have no difficulty digesting protein.

0032The vitamin content of the final product will

depend on the base ingredients used, the starter cul-

tures, and the processing conditions (especially heat

treatment). LAB can synthesize vitamins such as

folate in vitro and in vivo. Therefore, there may be

increased vitamin levels in some fermented products.

It is doubtful, however, whether these vitamins would

affect the vitamin status of healthy adults as their

bioavailability in the GIT is currently unknown.

0033The fermentation process does not generally affect

the mineral content of the product, although there

is some suggestion that bioavailability may be

enhanced. Like dairy milk, fermented dairy milk

products are excellent sources of a range of minerals

such as calcium, phosphorus, and zinc.

0034Traditional fermented milks and related products

can make a considerable contribution to the nutri-

tional status of some groups, particularly in develop-

ing countries, where they provide a good source of

nutrients (particularly protein) at a low cost.

tbl0004Table 4 Effect of lactic acid bacteria on composition of

fermented milk

Before fermentation After fermentation

Decreased Increased

Lactose Lactose Organic acids

Lactic acid

Galactose, glucose

Polysaccharides

Protein Protein Peptides

Free amino acids

Fat Fat Volatile and long-chain

free fatty acids

Vitamins Vitamins Vitamins (e.g., folate)

Adapted from Nakazawa Y and Hosono A (1992) Functions of Fermented

Milk Challenges for the Health Sciences. London: Elsevier.

FERMENTED MILKS/Other Relevant Products 2387