Fermented Milks: a Historical Food with Modern Applications — a Review
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European Journal of Clinical Nutrition (2002) 56, Suppl 4, S2–S15 ß 2002 Nature Publishing Group All rights reserved 0954–3007/02 $25.00 www.nature.com/ejcn Fermented milks: a historical food with modern applications — a review AY Tamime1* 1Dairy Science and Technology Consultant, Ayr, Scotland, UK Background: This paper was presented at the symposium which was organized by Instituto Danone Mexico in May 2001, and it provides an overview of the current scientific knowledge on fermented milks concerning the historical developments, manufacturing stages, classification of such products, and nutritional aspects. Particular attention has been paid to the human health benefits associated with the consumption of these products, the use of probiotic starter cultures and their industrial applications, and the significance of using a trained sensory panel for the evaluation of probiotic fermented milks made with different commercial blends of starter cultures. The paper also highlights the future research areas for the exploitation of starter microflora (Lactobacillus, Bifidobacterium and Enterococcus species) in fermented milk products. Conclusion: This review indicates that the complex metabolism of the starter cultures is well established; however, more information is still needed on specific microbial metabolites such as polymerization of milk sugars for the production of exopolysaccharides and the modification of the milk peptides and secretion of bacteriocins. More clinical studies are still required to establish the ‘functional’ health benefits of probiotic fermented milks to humans. Sponsorship: The visit to Mexico City was supported by Instituto Danone Mexico. European Journal of Clinical Nutrition (2002) 56, Suppl 4, S2 – S15. doi:10.1038/sj.ejcn.1601657 Descriptors: review; fermented milks; starter cultures; probiotic microflora; health benefits Introduction It is likely that the origin of these products was the Middle Fermented milks are widely produced in many countries. East and the Balkans, and the evolution of fermented milks This type of process is one of the oldest methods used to through the ages could be attributed to the culinary skills of extend the shelf-life of milk, and has been practised by the inhabitants living in these regions. Today’s fermented human beings for thousands of years. The exact origin(s) of milk products are manufactured in many countries, and the the manufacture of fermented milks is difficult to establish, stages of manufacture, which is still a complex process, but it is safe to assume that it could date to more than combine the art of such ancient craft and science (micro- 10 000 y ago as the way of life of humans changed from food biology and enzymology, physics and engineering, and gathering to food producing (Pederson, 1979). This change chemistry and biochemistry) together. also included the domestication of certain mammals such as This article summarizes the research findings on yoghurt the cow, sheep, goat, buffalo and camel; it is most likely that and probiotic fermented milk products made from cow’s the transition occurred at different dates in different milk over the past century. countries. However, archaeological evidence of certain civilizations (Sumerians, Babylonians, Pharos and Indians) suggests that they were well advanced in agriculture and in the production of fermented milks. Diversity of fermented milks Fermented milks are manufactured throughout the world, and approximately 400 generic names are applied to tradi- tional and industrialized products (Kurmann et al, 1992), but in actual essence the list may only include few varieties. In the 1980s, Kurmann (1984) attempted, in part, the classifica- *Correspondence: AY Tamime, Dairy Science and Technology Consultant, 24 Queens Terrace, Ayr KA7 1DK, Scotland, UK. tion of fermented milks into a ‘family tree’ (see Figure 1; E-mail: [email protected] Bylund, 1995), which was based primarily on the optimum Fermented milks — a review AY Tamime S3 Figure 1 The family tree of fermented milk types. Adapted from Kurmann (1984). growth requirements of the starter cultures (ie mesophilic (a) cloth bag or Berge system; (b) mechanical or nozzle and thermophilic microflora). separators; (c) ultrafiltration (UF); and (d) product formula- Nevertheless, taking into account the microorganisms tion (Tamime & Robinson, 1999). that dominate the product, including their principle metabolites, Robinson and Tamime (1990) proposed a scheme for the classification of fermented milks as follows: Patterns of consumption Until the 1950s, production and=or consumption of yoghurt lactic fermentations — (a) mesophilic type, eg cultured (ie natural type) was confined to communities in the Middle buttermilk, filmjo¨lk, ta¨tmjo¨lk and la˚ngofil; (b) thermo- East, the Balkans, India, Eastern Europe, to ethnic groups philic type, eg yoghurt, Bulgarian butter-milk, zabadi, living in different parts of the world, and to those who dahi; and (c) therapeutic or probiotic type, eg acidophilus perceived that the product was beneficial to health. How- milk, Yakult, ABT, Onka, Vifit); products within this ever, consumers’ attitudes towards yoghurt have changed, group constitute by far the largest number known possibly for the following reasons: (a) as refrigeration became worldwide; widespread worldwide, the product became widely distribu- yeast – lactic fermentations (kefir, koumiss, acidophilus ted and readily available on the market; (b) the introduction yeast milk); and of a ‘new’ generation of yoghurts (eg addition of fruits and mould – lactic fermentations (villi). sugar) gave the product an entirely fresh image and it Tamime and Marshall (1997) have detailed the manufac- became an inexpensive snack or dessert; and (c) the advent turing stages of these types of fermentations. However, the of incorporation of probiotic bacteria into the product have so-called fermented milk ‘drinks’ and=or beverages including enhanced the health benefits of fermented milks. the carbonated products should be classified separately Consumption figures reflect the expanding markets in rather than being known as fermented milks; such an some selected countries between 1970 and 1999 (Table 1). approach will minimize confusion among consumers. Never- Until the early 1990s, fermented milks were classified as theless, some closely related products are manufactured from buttermilk, yoghurt and others according to the statistical fermented milks by de-wheying, and some examples are data published by the International Dairy Federation, and labneh, skyr and ymer. The different methods available to such information provided consumption preferences of con- manufacture concentrated fermented milks are as follows: sumers in different countries; the current approach of European Journal of Clinical Nutrition Fermented milks — a review AY Tamime S4 Table 1 Per capita annual consumption (kg=head) of milk drinks increased from 1500 to > 91 000 tonnes between 1986 and and fermented products including yoghurt 1990 (Renard, 1998). Country 1975 1980 1990 1999 Australia 1.0 1.8 3.5 5.8 Definition and terminology of fermented milks Austria 7.9 9.8 10.4 15.1 including yoghurt Belgium 11.8 7.7 8.4 20.3 Canada 5.1 2.3 3.7 4.2 The existing legal standards or the provisional regulations of Chile NRa 1.4 3.9 6.7 yoghurt in many countries classify the product on the basis Czech=Slovakia 3.9 7.3 NR 20.0 of chemical composition or fat content (full, semi- Denmark 36.1 26.7 21.6 29.8 skimmed=medium or skimmed=low); the reviews by Robin- Federal Germany 16.5 10.1 14.2b 25.5b Finland 32.6 41.0 38.3 NR son and Tamime (1976), Pappas (1988), Anonymous (1989, France 9.6 9.3 16.4 27.4 1996), FAO=WHO (1990), and Tamime and Robinson (1999) Iceland 1.7 5.7 24.6 NR are recommended for further reading. Israel 14.1 14.3 NR 29.3 The International Dairy Federation (IDF, 1992a,b) pub- Italy NR 1.3 4.0 NR Japan 2.5 2.4 7.8 NR lished general standards of identity of fermented milks that Netherlands 24.7 27.3 32.5 NR could be brieflydefined as follows: ‘Fermented milks are Norway 9.8 10.1 14.9 19.9 prepared from milk and=or milk products (eg any one or Poland 3.2 2.0 NR 7.9 combinations of whole, partially or fully skimmed, concen- Spain 3.4 6.0 8.0 15.4 Sweden 24.1 23.5 29.1 30.2 trated or powdered milk, buttermilk powder, concentrated or Switzerland 16.4 14.8 19.0 NR powdered whey, milk protein (such as whey proteins, whey UK 1.7 2.8 4.4 NR protein concentrates, soluble milk proteins, edible casein USA 9.9 3.1 3.5c NR and caseinates), cream, butter or milkfat — all of which aNR ¼ not reported. have been manufactured from raw materials that have bData includes German Democratic Republic. been at least pasteurized) by the action of specific c Data for 1993. microorganisms, which results in a reduction of the pH Data compiled from Tamime and Robinson (1999) and IDF (2000). and coagulation. It is of interest that in some countries the fortification of milk components with dried dairy ingredi- ents during the manufacture, of yoghurt for example, is per capita consumption figures covers milk drinks and fer- against the existing legal standards. mented milks including yoghurt. It could be argued, how- Other IDF specifications include the following aspects: (a) ever, that this classification of these products may not the starter cultures shall be viable, active and abundant provide a clear picture or patterns of consumption. Further- ( 107 cfu=g) in the finished products at all times of sale for more, in some countries, the consumption of buttermilk is consumption; (b) these products may or may not be homo- not properly defined because: genized, must at least be pasteurized, contain certain per- mitted additives (optional), and have a shelf-life up to 30 traditional=natural buttermilk is the by-product of butter days at 4 – 7C; (c) post-fermentation heat treatment shall making from ripened or cultured butter; not be allowed; and (d) de-wheying after fermentation is cultured buttermilk is the fermentate of skimmed milk only permitted during the manufacture of concentrated followed by the addition of butter flakes; and fermented milk products such as labneh, ymer, skyr and sweet buttermilk is not fermented; hence the data for stragisto.