Fermented milks: a historical food with modern applications–a review

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* 1 Dairy 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 Fermented milks are widely produced in many countries. This type of process is one of the oldest methods used to extend the shelf-life of milk, and has been practised by human beings for thousands of years. The exact origin(s) of the manufacture of fermented milks is difficult to establish, but it is safe to assume that it could date to more than 10 000 y ago as the way of life of humans changed from food gathering to food producing (Pederson, 1979). This change also included the domestication of certain mammals such as the cow, sheep, goat, buffalo and camel; it is most likely that the transition occurred at different dates in different 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. *Correspondence: AY Tamime, Dairy Science and Technology Consultant, 24 Queens Terrace, Ayr KA7 1DK, Scotland, UK. E-mail: It is likely that the origin of these products was the Middle East and the Balkans, and the evolution of fermented milks through the ages could be attributed to the culinary skills of the inhabitants living in these regions. Today’s fermented milk products are manufactured in many countries, and the stages of manufacture, which is still a complex process, combine the art of such ancient craft and science (microbiology and enzymology, physics and engineering, and chemistry and biochemistry) together. This article summarizes the research findings on yoghurt and probiotic fermented milk products made from cow’s milk over the past century. Diversity of fermented milks Fermented milks are manufactured throughout the world, and approximately 400 generic names are applied to traditional 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 classification of fermented milks into a ‘family tree’ (see Figure 1; 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 and thermophilic microflora). Nevertheless, taking into account the microorganisms that dominate the product, including their principle metabolites, Robinson and Tamime (1990) proposed a scheme for the classification of fermented milks as follows:


lactic fermentations — (a) mesophilic type, eg cultured buttermilk, filmjölk, tätmjölk and långofil; (b) thermophilic type, eg yoghurt, Bulgarian butter-milk, zabadi, dahi; and (c) therapeutic or probiotic type, eg acidophilus milk, Yakult, ABT, Onka, Vifit); products within this group constitute by far the largest number known worldwide; yeast – lactic fermentations (kefir, koumiss, acidophilus yeast milk); and mould – lactic fermentations (villi). Tamime and Marshall (1997) have detailed the manufacturing stages of these types of fermentations. However, the so-called fermented milk ‘drinks’ and=or beverages including the carbonated products should be classified separately rather than being known as fermented milks; such an approach will minimize confusion among consumers. Nevertheless, some closely related products are manufactured from fermented milks by de-wheying, and some examples are labneh, skyr and ymer. The different methods available to manufacture concentrated fermented milks are as follows: (a) cloth bag or Berge system; (b) mechanical or nozzle separators; (c) ultrafiltration (UF); and (d) product formulation (Tamime & Robinson, 1999). Patterns of consumption Until the 1950s, production and=or consumption of yoghurt (ie natural type) was confined to communities in the Middle East, the Balkans, India, Eastern Europe, to ethnic groups living in different parts of the world, and to those who perceived that the product was beneficial to health. However, consumers’ attitudes towards yoghurt have changed, possibly for the following reasons: (a) as refrigeration became widespread worldwide, the product became widely distributed and readily available on the market; (b) the introduction of a ‘new’ generation of yoghurts (eg addition of fruits and sugar) gave the product an entirely fresh image and it became an inexpensive snack or dessert; and (c) the advent of incorporation of probiotic bacteria into the product have enhanced the health benefits of fermented milks. Consumption figures reflect the expanding markets in some selected countries between 1970 and 1999 (Table 1). Until the early 1990s, fermented milks were classified as buttermilk, yoghurt and others according to the statistical data published by the International Dairy Federation, and such information provided consumption preferences of consumers 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 and fermented products including yoghurt (...truncated)