Take home message

• Yoghurt belongs to the family of fermented milk products, nowadays mostly from highly heated cow’s milk, traditionally from sheep’s milk. It is one of the oldest dairy products, possibly originally from unpasteurised milk, made in warmer regions. You can see the latter especially in the two main bacterial species in yoghurt, which are known to grow at elevated temperatures.
• If you then thicken yoghurt by running it through a cloth or filtering it, you lose whey (moisture). The product is thicker, cottage cheese-like in consistency and is sold as Greek yoghurt. In Dutch it is called ‘hangop’ (= hanged in cloth).

One big family?

Fermented dairy products vary from region to region, if only in name. Yoghurt is part of this family of fermented products. Lactic acid is produced by the conversion of milk sugar. Sometimes acetic acid (by acetic acid-producing bacteria) or alcohol (fungi, yeasts) can be made as well. Traditional, regional names, according to Koroleva (1991), are: prostokvasha, varenec (central Russia), yoghurt (Turkey), kiselo mlyako or kyselo mleko (Bulgaria), Leben or Laban (Egypt, Syria, Lebanon), matsun, matsoni, ayran, kefir (Kazakhstan, Mongolia, Volga region), dadhi or dahi (India), or mast (Iran). Some products are mentioned as far back as 7,000 to 9,000 years ago (Chandan et al., 2017). According to these authors, the name ‘yoghurut’ is first mentioned in the 8^th century in Turkey. Incidentally, the Bulgarian term ‘kiselo mleko’ means leavened milk.

Yoghurt is mostly made with two bacterial species: Streptococcus thermopilus (ST) and Lactobacillus delbrueckii ssp. bulgaricus (LDB). The latter was known as Lactobacillus bulgaricus until 2014. LDB is a homofermentative lactic acid bacterium, meaning that they only ferment lactic acid from lactose without further by-products. LDB is found in several starter cultures, including yoghurt, as well as cheeses. Important is the temperature at which the bacteria grow. LDB and ST grow best at 35-41 ^oC (ST) or even 43-46 ^oC (LDB). Thermophilic is opposed to mesophilic, which are bacteria that are more likely to have their optimal growth at room temperature, 20-25 ^oC. The mesophilic and thermophilic distinction therefore rather splits sour dairy products (and cheeses) into two subgroups, roughly related to the warmer region of origin of India, and Eastern Europe (yoghurt, mountain cheese) and the cooler parts of the world, including north-western Europe (kefir, Camembert, Gouda cheese).

Discovery of Lactobacillus bulgaricus

The discoverer of LDB is the Bulgarian physician/microbiologist Stamen Grigoroff (1878-1945). It seems a reference to the Bulgarian origin of yoghurt, but the naming of the bacterium has much more to do with this Bulgarian as a discoverer. Incidentally, the discovery did not take place in Bulgaria, but in Geneva, Switzerland, where Grigoroff worked. The yoghurt he did bring with him from his homeland Bulgaria, was traditionally made in earthenware pots (Rukatka). Grigoroff found 3 species of bacteria in the fermented yoghurt from the earthenware pots, including the two bacteria mentioned above (LDB and ST). The Bulgarian female scientist Elitsa Stoilova wrote her PhD thesis ‘Producing Bulgarian Yoghurt: Manufacturing and Exporting Authenticity’ in 2014. Questions she asked, were: What is the authenticity, region of origin or terroir of yoghurt? According to which technology, recipe and with the milk of which animal species is yoghurt made?

Much of the info below comes from her (Stoilova, 2015).

Yoghurt was originally a small-scale farm product made mainly from sheep’s milk, not an industrial product. Industrial production from cow’s milk starts later, in the 1930s-40s. From Eastern Europe, yoghurt consumption spread across Western European countries and the US through the export of know-how, bacterial starter cultures and technology. The French company Danone uses the two bacterial species as starter cultures for their well-known yoghurts. Danone was founded by the Carosso family. Via Barcelona (1912), the yoghurt knowledge of Greek Isaac Carosso (1874-1939) ended up in France (1929), where he and with son Daniel (nickname: Dannon) were the first to sell yoghurt through pharmacies. Doctors provided further word-of-mouth advertising. It was promoted as a cure for diarrhoea and stomach complaints. People, living in cities at the time hardly drank ordinary raw cow’s milk (too unsafe, too many germs), but through the fermented yoghurt after heat treatment of the milk, milk consumption was gaining acceptance. The Nestlé company started the first manufacture of yoghurt in Constantinople, Turkey (1915). In their eyes, yoghurt was authentic, healthy and at the same time exotic, new. From Turkey, the first products were exported to Western Europe even then. Local knowledge was used for later factories in Switzerland and France. An important propagandist of yoghurt was Nobel laureate Ilya Ilych (Elie) Metchnikoff (1845-1916), a biologist/bacteriologist/immunologist of French/Russian origin who conducted his research at the renowned ‘Institut Pasteur’ in Paris since 1888. He pointed out the correlation of yoghurt consumption and reaching old age. Hotspots of people of advanced age were found in Greece, Serbia, Bulgaria and Romania, the so-called Centenarians. Almost always sheep farmers, who lived with and from their animals in mountainous areas and drank large quantities of traditionally fermented milk, daily. To oversimplify, they chose Bulgaria as the country of origin. This simplified the message through the advertisements. Half-truths sometimes became whole lies.

Historically, there have been more references of the health benefits of yoghurt and fermented milk. Yet traditional yoghurt with LDB and ST is not necessarily a probiotic. The definition of probiotic is that the bacteria in the product reach the gut alive, in larger quantities and are not killed and broken down en route during digestion. Therefore, there are also special probiotic yoghurts to which defined strains of bacteria are added, which do reach the gut alive (including Bifido bacteria, Lactobacillus casei and Lactobacillus acidophilus), (Chandan et al., 2017).

Dickmilch, clabbermilk, yoghurt

When do you call something spontaneously acidified milk, when does it become yoghurt? Fermentation of milk is ancient, and when you put raw milk aside, spontaneous acidification occurs. Acidified milk was no longer liquid, the protein flocculated due to the low pH (under pH 4.5), milk became thick and slightly sour in taste. This occurs most easily, if the milk is ‘contaminated’ from wooden utensils (cracks, seams), or other bacterial biofilms the milk encounters (originally goat skins, etc where milk was stored). When the temperature is above 20 ^oC, acidification is within 24 hours.

Modern yoghurt is made from ‘cooked’ milk. This makes it nice and thick, and the yoghurt contains mainly thermophilic bacteria. This may indicate that yoghurt originated earlier from warmer regions (southern Europe, pre-Asia and India). The further west and the further north, the more likely you are to find mesophilic bacteria.

Both boiling and the use of bacteria selected in laboratories, which were used in starter cultures, are an important contribution to the scientific standardisation of the yoghurt process. This kind of intervention (high-temperature-pasteurisation of the milk plus the addition of freeze-dried starter cultures) is now common for the mass production of all industrial dairy products.

Greek yoghurt

Greek yoghurt is yoghurt that has hung in a cloth for a while to drain (Tamime et al., 2014). The dried skins of the animals were used used to serve as drainage to drain whey. This allowed the yoghurt to thicken greatly. Greek yoghurt is therefore of a thicker consistency than regular yoghurt. When you make Greek yoghurt from (partially) skimmed milk, you get a stronger emphasis on the protein proportion. Since the fat to protein ratio of different animal species is not the same either, you also get other types of Greek yoghurt from fermented buffalo milk, sheep’s milk, goat’s milk or cow’s milk. In English, Greek yoghurt is called ‘strained yoghurt’ (Tamime et al., 2014). In modern processing whey is extracted by centrifuging and/or filtering the product. Icelandic Skyr contains 0% fat and is a filtered/centrifuged product made from skimmed cow’s milk after lactic acid fermentation. Curiously, such Greek yoghurt variants made from skim milk are thicker in consistency and richer in protein than the plain, full-fat yoghurt (Chandan et al., 2017). Table 1 shows examples, what the differences in contents are for different yoghurts (plain or Greek) with different fat content in the milk. From this you can easily deduce, how skimmed milk becomes a protein-rich product after filtration/ centrifugation or as a hangup. Other authors believe that Greek yoghurt should be further thickened than indicated in Table 1, citing a limit of 23-25 g total dry matter (fat, protein, lactate) corresponding to a moisture content of over 75% (Tamime et al., 2014). Thickened, or condensed, or strained varieties of their local yoghurt are known in many countries. Well-known names are Skyr and Ymer. People also have such products further acidified and/or salt added with the aim of longer and better preservation.

A higher protein share can also be achieved by adding milk protein before adding the starter culture. This makes the yoghurt a bit thicker in consistency anyway, irrespective of whether it was hanged out in cloth.

Table 1. Plain yoghurt and Greek yoghurt with different fat contents: energy, protein, fat and moisture content per 100 g of product (from: Chandan et al., 2017).

per 100g of product		Yoghurt			Greek yoghurt
	Full-fat	2%	Skimmed	Full-fat	2%	Skimmed
Water (%)	87.9	85.1	85.2	81.3	83.6	85.1
Protein (g)	3.47	5.25	5.73	9.00	9.95	10.19
Fat (g)	3.25	1.55	0.18	5.00	1.92	0.39
Energy (kcal)	61	63	56	97	73	59
Ratio protein/fat	107	339	3183	180	518	2613

The appeal of Greek yoghurt probably lies in its high protein content. Especially if you use skim milk, you eat proportionally a lot of protein and little fat. It is still assumed, that protein is healthy and the (saturated) milk fat is unhealthy (although we disagree with this point of view). Advertisers boast about the ‘creamy’ consistency of fat-free Skyr, its contribution to an athletic life. No mention is made of the high heating of the starting milk (>95^o C, 10 min), which is normal in yoghurt production. This at least denatures all whey proteins and partially binds them to milk sugars (Maillard reaction). In terms of immunological health, strangely enough, it is precisely the unchanged, undenatured whey proteins that make the difference in allergic and asthma outcomes (Abbring et al. 2019).

Literature

• Abbring, S., Hols, G., Garssen, J., & van Esch, B. C. (2019). Raw cow’s milk consumption and allergic diseases–the potential role of bioactive whey proteins. European Journal of Pharmacology, 843, 55-65.
• Chandan, R. C., Gandhi, A., & Shah, N. P. (2017). Yogurt: Historical background, health benefits, and global trade. In Yogurt in health and disease prevention (pp. 3-29). Academic Press.
• Koroleva, N. S. (1991). Products prepared with lactic acid bacteria and yeasts. Therapeutic properties of fermented milks., 159-179.
• Stoilova, E. (2015). The bulgarianization of yoghurt: Connecting home, taste, and authenticity. Food and Foodways, 23(1-2), 14-35.
• Tamime, A. Y., Hickey, M., & Muir, D. D. (2014). Strained fermented milks–A review of existing legislative provisions, survey of nutritional labelling of commercial products in selected markets and terminology of products in some selected countries. International Journal of Dairy Technology, 67(3), 305-333.