Introduction
Ten thousand years ago, after the onset of agriculture, man’s dietary adaptation to a few plant and animal species gave rise to new techniques in order to enhance the nutrient composition and, often simultaneously, rid their foodstuffs of their antinutritional effects( Reference Marshall and Mejia 1 , Reference Prajapati and Nair 2 ). At the same time, settlement forced humans to collect foods as a store of supplies to secure food availability during periods of bad weather, when fresh food and safe drinking water were not readily available( Reference Standage 3 ). Especially for alcoholic beverages, such as beer and wine, data from recent research support their contribution to the transition of our ancestors from hunter–gatherers to farmers( Reference Marshall and Mejia 1 – Reference Tamang and Samuel 4 ). Based on archaeological and archaeobotanical findings, it is generally believed that over 9000 years ago individuals of the globe were already fermenting beverages( Reference McGovern, Zhang and Tang 5 ). For instance, remnants in jars and vessels suggest that winemaking was popular in Neolithic Egypt and Middle East( Reference Marshall and Mejia 1 , Reference Prajapati and Nair 2 , Reference Leroy and De Vuyst 6 ). Overall, food fermentation stands as a remarkable benchmark in the history of human societies.
Historically, besides their role in human nourishment, fermented beverages have found other uses as well. They have been used as exchangeable products for labourers who worked in the construction of pyramids in Egypt and in royal cities and irrigation networks in ancient Central American cultures( Reference Marshall and Mejia 1 , Reference Prajapati and Nair 2 ). Furthermore, many ancient cultures have used alcoholic fermented drinks as medicines; in ancient Egypt, Rome and Greece as well as in ancient Mesopotamia and China, fermented beverages were used to relieve pain and to prevent or treat diseases( Reference Marshall and Mejia 7 ). Koumiss, a traditional alcoholic fermented beverage of Kazakh nomads made from mares’ milk had been used by Russian doctors for the treatment of tuberculosis and diarrhoea( Reference Tamang 8 ). Sorghum beer, a good niacin source, has helped to prevent pellagra in Southern Africa( Reference Marshall and Mejia 1 , Reference Prajapati and Nair 2 ). It has also been observed that children who consumed the dregs of sorghum beer were protected against the development of pellagra( Reference Battock and Azam-Ali 9 ). In the United Republic of Tanzania, it has been observed that children who consumed fermented gruels showed a decrease in the number of reports for diarrhoea by one-third as opposed to those who were fed with unfermented gruels; this difference was attributed to the inhibitory effect of the microbiota of fermentation towards pathogenic bacteria( Reference Marshall and Mejia 1 , Reference Prajapati and Nair 2 ).
Fermentation cοntributes to food security, especially in agro-pastoralist societies. As an example, in Indonesia, the wastes of groundnut press cake and tapioca are often fermented to produce nutritious foods, namely tempte-bongrek and ontjom, foods that are important in the daily regimen of the poorest individuals( Reference Tamang 8 ), while koumiss had been used as a safe and easy to transport beverage for nomadic populations of Central Asia, who had to travel very often to places with variations in climatic and environmental conditions( Reference Battock and Azam-Ali 9 ). Kawal, a fermented product made of the leaves of a wild African legume, is believed to have helped children and adults in Sudan endure the 1983–1985 famine( Reference Tamang 8 ).
Fermentation enables the preservation of foods as well as the transformation of the raw material into a new product with unique sensorial properties( Reference Tamang and Samuel 4 , Reference Rolle and Satin 10 – Reference Holzapfel 12 ) and enhanced nutritional value. Food and beverages that are prepared via a fermentation process represent an important part of human nutrition in practically every food culture around the world( Reference Tamang and Samuel 4 ). Fermented/pickled fruits and vegetables are very popular in many regions of Europe, Asia, America and Africa and Middle East( Reference Josephsen and Jespersen 13 ). Fermented fruit juices, tea leaves and products in brine are widely consumed in Asia. Fermented cereals, roots and tubes, such as pickles, porridges and gruels, make a major contribution to dietary staples in countries across Africa, Asia, Europe and Latin America( Reference Josephsen and Jespersen 13 ), while fermented seeds and fish are also widespread in many regions around the globe( Reference Josephsen and Jespersen 13 ). With regard to fermented foods in liquid form, in Western societies, beverages made with alcohol-producing yeasts, such as beers and wines, are the dominant ones( Reference Standage 3 , Reference De Garine 14 ). Alcoholic drinks played an important role throughout most of Western civilisation’s history as a source for hydration and energy; however, in most recent history, they are responsible for many major health and social destructors. But fermentation need not always result in a beverage with alcoholic content. Low-alcoholic fermented beverages (LAFB) and non-alcoholic fermented beverages (NAFB) have been treasured as major dietary constituents in numerous European countries because of their keeping quality under ambient conditions and prolonged shelf-life, thereby contributing to food security and improving food safety( Reference Sõukand, Pieroni and Biró 15 ). The use of the terms ‘alcoholic beverage’, ‘LAFB’ and ‘NAFB’ is subject to varying regulations in different European countries. According to EU Regulation 169/2011 on the provision of Food information to consumers and the European Parliament Resolution 2015/2543 (RSP) an ‘alcoholic beverage’ contains an ‘alcoholic strength by volume’ (ABV; the number of litres of ethanol contained in 100 litres of wine, both volumes being measured at a temperature of 20°C) of more than 1·2%, whereas a ‘low-alcoholic beverage’ refers only to beverages which have an ABV of 1·2 % or less. For the majority of the European countries, the limit of ABV for a ‘non-alcoholic beverage’ is considered 0·5 %.
The diversity of traditional fermented beverages in Asia and Africa has been well described in review articles and textbooks( Reference Tamang and Samuel 4 , Reference McGovern, Zhang and Tang 5 , Reference Steinkraus 11 , Reference Sõukand, Pieroni and Biró 15 , Reference Steinkraus 16 ). For example, the rich legacy and diversity of traditional fermented foods and beverages of the Himalayas have recently been recorded by Tamang & Samuel( Reference Tamang and Samuel 17 ). However, the scientific literature contains limited information on LAFB and NAFB prepared and consumed by European populations. Thus, the primary purpose of the present review is to provide an overview of the research regarding traditional LAFB and NAFB in European cuisines, including a documentation of the different types and a record of their modern and traditional names. Second, this review aims at comprehensively presenting information on the raw material undergoing the fermentation, the microbiota involved, as well as the health effects, dietary importance and cultural aspects of the endproducts. The results of this research are summarised in the tables, but selected traditional beverages are presented extensively. Finally, because in the last decades the food and beverage industry has focused on the revival and re-introduction of these indigenous beverages, their place in the European market and their perspectives and innovations are discussed.
Diversity of traditional low-alcoholic and non-alcoholic fermented beverages
Traditional LAFB and NAFB constitute an integral part of food culture of many European countries. They represent socially accepted products for habitual as well as ritual consumption. A diversity of traditional LAFB and NAFB( Reference Marshall and Mejia 1 , Reference Battock and Azam-Ali 9 ) are produced from both edible and inedible raw materials in many European countries. Some of these beverages are well documented in the scientific literature, but for most of them, the existing information with regard to the names used (traditional and modern), the substrate and microbiota of fermentation involved, the spread of their consumption, the preparation method(s), the nutrient composition and perceptions on their nutritional value is incomplete. A wide range of substrates, including milk, cereals, fruits and vegetables, are used for the production of LAFB and NAFB. These substrates provide the criteria for the integration of traditional LAFB and NAFB into different categories. Representative examples of traditional LAFB and NAFB are presented in each category of these beverages.
Traditional fermented low-alcoholic and non-alcoholic milk-based beverages
Kefir
Kefir or kefyr (in Central Asia and Middle East) or kephir/kiaphur/kefer/knapon/kepi/kippi (in the Balkan–Caucasian region) is one of the oldest milk-based fermented beverages( Reference Battock and Azam-Ali 9 , Reference Tamang and Samuel 17 – Reference Fondén, Leporanta and Svensson 19 ) (Table 1). It can be made from any type of milk (goats’, sheep’s, cows’, camel, buffalo) and kefir grains( Reference Battock and Azam-Ali 9 , Reference Tamang and Samuel 17 ). Nowadays, novel varieties are also being made from milk substitutes, such as soya, rice and coconut milk( Reference Mayo, Ammor and Delgado 18 , Reference Altay, Karbancıoglu-Güler and Daskaya-Dikmen 20 – Reference Panesar 23 ). The word ‘kefir’ originates from the Turkish word ‘keyif”, which means ‘good feeling’ and is believed to describe the sense experienced when consumed( Reference Altay, Karbancıoglu-Güler and Daskaya-Dikmen 20 , Reference Lopitz-Otsoa, Rementeria and Elguezabal 24 ). It has been traditionally prepared by shepherds in the Caucasus mountains( Reference Altay, Karbancıoglu-Güler and Daskaya-Dikmen 20 , Reference Marsh, Hill and Ross 22 , Reference Lopitz-Otsoa, Rementeria and Elguezabal 24 , Reference Özdestan and Üren 25 ) in bags made from animal hides, oak barrels or earthenware pots( Reference Fondén, Leporanta and Svensson 19 ). Kefir’s production and consumption originate from the countries of Eastern Europe, especially the Balkan–Caucasian region and Russia( Reference Battock and Azam-Ali 9 , Reference Steinkraus 11 , Reference Mayo, Ammor and Delgado 18 , Reference Marsh, Hill and Ross 22 , Reference Özdestan and Üren 25 , Reference Chandan 26 ). It has been widely consumed in Soviet countries for centuries; however, nowadays it is increasingly popular in Japan, the USA, the Middle East and Africa( Reference Battock and Azam-Ali 9 ).
Table 1 Examples of traditional milk-based low-alcoholic and non-alcoholic fermented beverages consumed in European countries
LAB, lactic acid bacteria; EPS, exopolysaccharides.
The type and amount of milk and the complex interactions between yeast and lactic acid bacteria (LAB) may influence the sensorial and textural properties of kefir ( Reference Altay, Karbancıoglu-Güler and Daskaya-Dikmen 20 ). Specifically, its flavour depends on the metabolism of LAB and yeast. Ethanol has little impact on flavour but may contribute to the aroma( Reference Fondén, Leporanta and Svensson 19 ). Kefir is a self-carbonated (some effervescence caused by carbon dioxide), slightly foamy and viscous beverage, with a uniform creamy and elastic consistency and sour, acidic and slightly alcoholic flavour( Reference Tamang and Samuel 17 , Reference Fondén, Leporanta and Svensson 19 , Reference Altay, Karbancıoglu-Güler and Daskaya-Dikmen 20 , Reference Panesar 23 , Reference Lopitz-Otsoa, Rementeria and Elguezabal 24 ). It also has a perceptible yeast aroma and white or yellowish colour( Reference Tamang and Samuel 17 , Reference Panesar 23 ).
Kefir is regarded as an easily digested, effervescent fermented milk beverage and is esteemed for its nutritional value( Reference Lopitz-Otsoa, Rementeria and Elguezabal 24 , Reference Wolfe and Dutton 27 , Reference Melo and Silva 28 ). It typically contains (per 100 g) 3·0–3·4 g of protein, 1·5 g of fat and 2·0–3·5 g of lactose (after the fermentation stage). However, the lactic acid content may range between 0·6 and 1·0 ml per 100 ml of the final product( Reference Fondén, Leporanta and Svensson 19 ). Kefir’s vitamin and amino acid content increases during fermentation via biological enrichment( Reference Kabak and Dobson 21 , Reference Melo and Silva 28 ). The fermenting action of kefir bacteria and yeasts increase the biological value of milk, increasing the synthesis of B group vitamins. It has been proposed by many researchers that during kefir fermentation pyridoxine, vitamin B12, folic acid and biotin are produced by the microbiota( Reference Kneifel and Mayer 29 , Reference Liutkevičius and Šarkinas 30 ), but it depends on the type of milk and the microbiota composition( Reference Ahmed, Wang and Ahmad 31 ). The incorporation of Propionibacterium freudenreichii strains in the kefir microbiota may enrich the product with vitamin B12 ( Reference Van Wyk, Witthuhn and Britz 32 ). Its alcoholic content is usually <2 % (<0·3 % (w/v) for Turkish kefir)( Reference Özdestan and Üren 25 ).
Typically, the raw material used for the production of kefir is cows’ milk, fortified with cheese whey (at homemade scale)( Reference Paraskevopoulou, Athanasiadis and Blekas 33 ) or ultrafiltered skimmed milk (at industrial scale)( Reference Fondén, Leporanta and Svensson 19 ). Two methods have been described for kefir production, the traditional (authentic) and the industrial (commercial)( Reference Lopitz-Otsoa, Rementeria and Elguezabal 24 , Reference Chandan 26 ). The type of fermentation observed in kefir is the result of a yeast–lactic fermentation. Traditionally, kefir grains are added to milk, left at room temperature for fermentation for 18–24 h; the grains are then removed and can be used in a new fermentation cycle. The resulting fermented milk is thus ready for consumption( Reference Lopitz-Otsoa, Rementeria and Elguezabal 24 ). Commercial types of kefir may be blended with sugar and fruit juices or flavours( Reference Mayo, Ammor and Delgado 18 ).
Microbiota identification shows that kefir is a symbiotic combination of bacteria (about 83–90 % LAB and acetic acid bacteria), lactose-fermenting and lactose-negative yeasts (about 10–17 %), such as Naumovozyma, Kluyveromyces, Kazachstania, other bacterial groups and possibly moulds (Geotrichum candidum), bound within a polysaccharide matrix, known as kefir grains or kefiran, made of casein and complex sugars( Reference Fondén, Leporanta and Svensson 19 , Reference Kabak and Dobson 21 , Reference Panesar 23 , Reference Lopitz-Otsoa, Rementeria and Elguezabal 24 , Reference Wolfe and Dutton 27 ). Kefir grains are filtered off after each use and reused for the inoculation of the next batch( Reference Chandan 26 ). Kefir milk possesses a lower diversity of bacteria compared with kefir grains. Only four phyla have been identified in kefir samples, Actinomycetes, Bacteroidetes, Firmicutes, Proteobacteria, with Bacteroides traced only in kefir milks( Reference Marsh, O’Sullivan and Hill 34 ). Bacteria involved in kefir’s production belong to the genera Lactococcus, Lactobacillus, Leuconostoc and Acetobacter ( Reference Marsh, Hill and Ross 22 ). Lactobacillus is the dominant genus in the kefir grains while Lactococcus and Leuconostoc are prevalent in kefir milk. Pyrosequencing analysis of kefir samples has revealed that the Acetobacter genus is not always detected, indicating that it is not required for the process of fermentation, contributing probably in other characteristics of the product. Bifidobacteriaceae were traced only in a minor number of kefir grains. High-throughput sequencing enables the detection of bacterial genera associated with the intestinal microbiota, rarely found in kefir samples and some of them (Faecalibacterium, Allistipes), identified for the first time in kefir ( Reference Marsh, O’Sullivan and Hill 34 ). Because many of the LAB in the kefir grains, such as Lb. acidophillus, Lb. helveticus, Lb. casei, Pediococcus dextrinicus, P. acidilactici, P. pentosaceus, etc.( Reference Altay, Karbancıoglu-Güler and Daskaya-Dikmen 20 , Reference Tamang, Watanabe and Holzapfel 35 ), are known to have probiotic properties, kefir is also being regarded as a potentially probiotic product( Reference Mayo, Ammor and Delgado 18 , Reference Kabak and Dobson 21 , Reference Lopitz-Otsoa, Rementeria and Elguezabal 24 , Reference Özdestan and Üren 25 , Reference Melo and Silva 28 , Reference Magalhães, Pereira and Nicolau 36 , Reference Tamang, Shin and Jung 37 ). The microbial counts of traditional and commercial kefir are different. The carbohydrate, fat and protein content of the milk used can affect the microbiota profile( Reference Altay, Karbancıoglu-Güler and Daskaya-Dikmen 20 ). The main metabolites of the kefir fermentation are lactic acid, produced by LAB and ethanol, carbon dioxide, produced mainly by the yeasts but also by heterofermentative LAB. Carbon dioxide content increases during fermentation as the pH drops. If the fermentation is carried out for longer than 24 h, carbon dioxide production plateaus after 48 h. The concentration of carbon dioxide in traditional kefir varies between 0·65 g/l (grain free, 24 h)–1·33 g/l (grain fermented, 24 h)( Reference Clementi, Gobbetti and Rossi 38 ). Also, volatile acids, acetaldehyde, diacetyl and acetoin (flavour compounds) are found in smaller quantities, while biogenic amines have been traced in kefir samples but in very low amounts, below the allowable limits( Reference Fondén, Leporanta and Svensson 19 ).
Ayran
Ayran is a dairy NAFB (Table 1). It is a salt-containing yoghurt drink made from cows’ milk or other types of milk( Reference Altay, Karbancıoglu-Güler and Daskaya-Dikmen 20 , Reference Kabak and Dobson 21 ). Ayran is consumed in Turkey( Reference Altay, Karbancıoglu-Güler and Daskaya-Dikmen 20 – Reference Marsh, Hill and Ross 22 ), Bulgaria, Macedonia, Kazakhstan, Kyrgyzstan and Azerbaijan( Reference Chandan 26 ). Beverages that are similar to ayran include ayrani (Cyprus), jugurt/eyran (Turkey), dhalle (Albania), ayryan (Bulgaria) and ariani (Greece)( Reference Chandan 26 ). Ayran is a low-viscosity drink, easily digestible and consumed mainly during the summer months( Reference Altay, Karbancıoglu-Güler and Daskaya-Dikmen 20 , Reference Kabak and Dobson 21 ). Its composition depends on the type of milk used, the milk’s fat content and the dilution rate used; for instance, its protein content by weight may range between 1·5 and 3·5 %( Reference Altay, Karbancıoglu-Güler and Daskaya-Dikmen 20 ).
Ayran is traditionally prepared by blending yoghurt with water (30–50 %) and salt (0·5–1%), is produced daily and consumed fresh (homemade version)( Reference Altay, Karbancıoglu-Güler and Daskaya-Dikmen 20 ). It can also be produced industrially by the addition of Streptococcus thermophilus and Lactobacillus delbrueckii subsp. bulgaricus to standardised milk (industrial version)( Reference Altay, Karbancıoglu-Güler and Daskaya-Dikmen 20 , Reference Kabak and Dobson 21 ). The resulting microbial composition of homemade ayran is generally similar to that of yoghurt( Reference Altay, Karbancıoglu-Güler and Daskaya-Dikmen 20 , Reference Marsh, Hill and Ross 22 ). Microbiota of fermentation consists of LAB bacteria such as Lb. delbrueckii subsp. bulgaricus and S. thermophilus, with microbial populations varying due to several factors, such as the increase of the acidity( Reference Altay, Karbancıoglu-Güler and Daskaya-Dikmen 20 , Reference Marsh, Hill and Ross 22 ). The population of yoghurt bacteria in industrially produced ayran is higher than in homemade ayran ( Reference Altay, Karbancıoglu-Güler and Daskaya-Dikmen 20 ). Some strains of Lb. delbrueckii subsp. bulgaricus, which are used as a starter culture, may produce bitter peptides( Reference Altay, Karbancıoglu-Güler and Daskaya-Dikmen 20 ). Furthermore, lactic acid may be produced by the starter cultures, even during storage (post-acidification).
Buttermilk
Buttermilk (or clabbered milk) can be classified as a LAFB and is usually made from cows’ milk and, less often, from buffalo milk( Reference Battock and Azam-Ali 9 , Reference Panesar 23 ) (Table 1). Buttermilk’s preparation has been always associated with butter production. For this reason, it is consumed in regions where butter-making is common( Reference Fondén, Leporanta and Svensson 19 ), for example, Russia, Bulgaria (urgutnik made from sheep’s milk), Ireland (clabber made from sheep’s milk), Southern Scandinavia (the Finnish kirnupiima made from sheep’s milk) and Hungary (savanyutez made from sheep’s milk), particularly during the summer months( Reference Battock and Azam-Ali 9 , Reference Fondén, Leporanta and Svensson 19 , Reference Park and Guo 39 ). It is also consumed in the USA, Canada, the Middle East, Egypt, Ethiopia, India, Australia and New Zealand( Reference Battock and Azam-Ali 9 ). Natural buttermilk is different from Bulgarian buttermilk or acidophilus milk( Reference Leatherman and Wilster 40 ). Nowadays, buttermilk has been mostly replaced by its modern version, cultured buttermilk( Reference Mayo, Ammor and Delgado 18 , Reference Fondén, Leporanta and Svensson 19 ). Buttermilk is a fluid of very low viscosity (due to the mechanical treatment, the churning of the cream)( Reference Fondén, Leporanta and Svensson 19 ) and can be slightly yellowish in colour (usually due to the addition of a colouring agent during butter production). It has a sour taste( Reference Battock and Azam-Ali 9 ). Besides being used as a beverage, buttermilk can be used in cooking as well, in the same way as sour cream.
Traditionally, buttermilk is produced right after milk or cream is churned( Reference Mayo, Ammor and Delgado 18 , Reference Leatherman and Wilster 40 ), as a part of the butter-making process( Reference Mayo, Ammor and Delgado 18 ), while the overall quality of buttermilk is entirely dependent on how the process of butter making is optimised( Reference Fondén, Leporanta and Svensson 19 ). The microbiota involved in the fermentation process includes mesophilic LAB( Reference Battock and Azam-Ali 9 ). The micro-organisms present in the starter culture are similar to those used for the production of surmjolk, a traditional fermented milk consumed mainly in the Southern and Western parts of Nordic countries( Reference Fondén, Leporanta and Svensson 19 ). The optimal temperature of buttermilk production is 17–22°C, while this range of temperature reassures the growth of mesophilic LAB( Reference Mayo, Ammor and Delgado 18 ).
Traditional fermented non-alcoholic or low-alcoholic cereal-based beverages
Boza
Boza, a cereal-based fermented beverage, is a type of millet beer. In this respect, its origin can be traced back to 8000–9000 years ago, when cereals were first fermented by man to produce beverages( Reference Arici and Daglioglu 41 ) (Table 2). The word boza derives from the Persian word buze ( Reference Leatherman and Wilster 40 ), which means millet. It is made from wheat or rice semolina or from a combination of rye, oat, barley and millet flour for best quality and taste( Reference Marsh, Hill and Ross 22 , Reference Arici and Daglioglu 41 ). Maize can also be one of the raw materials( Reference Altay, Karbancıoglu-Güler and Daskaya-Dikmen 20 , Reference Marsh, Hill and Ross 22 , Reference Albuquerque, Costa and Sanches-Silva 42 – Reference Yeğin and Üren 45 ) mixed with sugar( Reference Sõukand, Pieroni and Biró 15 , Reference Kabak and Dobson 21 , Reference Blandino, Al-Aseeri and Pandiella 44 , Reference Prado, Parada and Pandey 46 ). Boza is widely consumed in Turkey( Reference Altay, Karbancıoglu-Güler and Daskaya-Dikmen 20 – Reference Marsh, Hill and Ross 22 , Reference Blandino, Al-Aseeri and Pandiella 44 – Reference Prado, Parada and Pandey 46 ) and in other countries of the Balkan Peninsula, such as Bulgaria (Sofia, Varna, Burgas)( Reference Altay, Karbancıoglu-Güler and Daskaya-Dikmen 20 – Reference Marsh, Hill and Ross 22 , Reference Albuquerque, Costa and Sanches-Silva 42 – Reference Blandino, Al-Aseeri and Pandiella 44 , Reference Prado, Parada and Pandey 46 , Reference Todorov, Botes and Guigas 47 ), Albania( Reference Kabak and Dobson 21 , Reference Blandino, Al-Aseeri and Pandiella 44 , Reference Prado, Parada and Pandey 46 ), Romania( Reference Kabak and Dobson 21 , Reference Gotcheva, Pandiella and Angelov 43 , Reference Blandino, Al-Aseeri and Pandiella 44 , Reference Prado, Parada and Pandey 46 ), South Russia, Fyrom( Reference Kabak and Dobson 21 ), Anatolia, Middle East and Northern Persia( Reference Arici and Daglioglu 41 ). Braga or brascha is a similar beverage consumed in East European countries, Busa is another similar beverage consumed in the Balkans (cocoa is included in the standard boza recipe), while bouza is also a similar beverage consumed in Egypt( Reference Arici and Daglioglu 41 ). It is produced both at an artisanal and industrial scale( Reference Marsh, Hill and Ross 22 , Reference Yeğin and Üren 45 ). In several Balkan countries, boza may be consumed on a daily basis( Reference Todorov, Botes and Guigas 47 ), mainly in winter time( Reference Kabak and Dobson 21 ). In Turkey, boza is considered to be beer’s ancestor and is sometimes served with cinnamon and roasted chickpeas( Reference Arici and Daglioglu 41 , Reference Yeğin and Üren 45 ).
Table 2 Examples of traditional cereal-based low-alcoholic and non-alcoholic fermented beverages consumed in European countries
LAB, lactic acid bacteria.
Boza is a viscous beverage with a form of colloid suspension( Reference Kabak and Dobson 21 ), with a slightly sour or sweet flavour (depending on its acid content)( Reference Leatherman and Wilster 40 , Reference Albuquerque, Costa and Sanches-Silva 42 , Reference Gotcheva, Pandiella and Angelov 43 , Reference Todorov, Botes and Guigas 47 ), an acidic–alcoholic odour and pale yellow or from light to dark beige colour( Reference Altay, Karbancıoglu-Güler and Daskaya-Dikmen 20 , Reference Arici and Daglioglu 41 ). Its odour and taste are affected by metabolites deriving via alcohol fermentation( Reference Altay, Karbancıoglu-Güler and Daskaya-Dikmen 20 ). Boza’s variations in composition and nutritive value are the result, first, of the utilisation of different types and amounts of cereal products (raw materials) and, second, of spontaneous fermentation conditions( Reference Altay, Karbancıoglu-Güler and Daskaya-Dikmen 20 ). The selection of raw materials is very important, as these affect the degree of fermentability, viscosity and DM content( Reference Altay, Karbancıoglu-Güler and Daskaya-Dikmen 20 ). Boza is a source of, protein, carbohydrate, fibre and vitamins, including thiamine, riboflavin, pyridoxine and niacin( Reference Kabak and Dobson 21 , Reference Arici and Daglioglu 41 ). Boza’s alcoholic content is either not detectable or up to 1·5 % (w/v)( Reference Sõukand, Pieroni and Biró 15 , Reference Altay, Karbancıoglu-Güler and Daskaya-Dikmen 20 , Reference Kabak and Dobson 21 , Reference Gotcheva, Pandiella and Angelov 43 ). Turkish boza, in particular, has an alcoholic content of 0·03–0·39 % (w/v)( Reference Yeğin and Üren 45 ) or lower than 2 % by volume in both the sour and sweet versions, according to the Turkish Boza Standard, TS 9778( Reference Arici and Daglioglu 41 ).
Boza’s preparation involves six stages: preparation of raw materials, boiling, cooling, straining, addition of sugar and fermentation( Reference Arici and Daglioglu 41 ). Another option for its production is the use of previously fermented boza as inoculum. The types of fermentation observed are lactic acid fermentation by LAB and alcohol fermentation by yeasts. Microbiota identification of boza shows that it mainly consists of LAB (most of them lactobacilli, such as Lactobacillus plantarum, Lb. acidophilus, Lb. fermentum, Lb. coprophilus, Leuconostoc raffinolactis, Ln. mesenteroides and Ln. brevis) and yeasts (such as Saccharomyces cerevisiae, Candida tropicalis, C. glabrata, Geotrichum penicillatum and G. candidum)( Reference Fondén, Leporanta and Svensson 19 , Reference Leatherman and Wilster 40 , Reference Albuquerque, Costa and Sanches-Silva 42 , Reference Gotcheva, Pandiella and Angelov 43 , Reference Prado, Parada and Pandey 46 ). Generally, LAB dominate; in the Bulgarian boza especially, the average LAB:yeasts ratio amounts to 2·4( Reference Blandino, Al-Aseeri and Pandiella 44 ). Boza is considered to be a rich source of probiotic bacteria, such as Lb. plantarum, Lb. paracasei, Lb. rhamnosus and Lb. pentosus ( Reference Altay, Karbancıoglu-Güler and Daskaya-Dikmen 20 ). Some of these bacteria are known to exhibit pronounced auto-aggregation properties as well as antiviral and antibacterial activity( Reference Todorov, Botes and Guigas 47 ).
Kvass
Kvass is a cereal-based beverage, used mostly as a type of soft drink( Reference Marsh, Hill and Ross 22 , Reference Dlusskaya, Jänsch and Schwab 48 , 49 ) (Table 2). Traditionally, it is produced from rye and barley malt, rye flour and stale rye bread( Reference Dlusskaya, Jänsch and Schwab 48 ). Another version of kvass, kvass southern, is made from water, rye bread, sugar, yeast, juniper berries (Juniperus communis L.) and raisins( Reference Albuquerque, Costa and Sanches-Silva 42 , Reference Costa, Albuquerque and Sanches-Silva 50 ). Mint kvass, a traditional Russian drink, is another version, which is made from stale dark rye bread( 49 ), to which water, sugar, dried yeast, fresh mint leaves and raisins or sultanas are added( 49 ). The mint can be omitted or replaced by honey or lemon peel. Kvass has normally a low alcoholic content, 1 % or even less; if it exceeds this concentration, then is considered spoiled( Reference Marsh, Hill and Ross 22 , Reference Dlusskaya, Jänsch and Schwab 48 ). Kvass is a very popular beverage in the countries of the former Soviet Union, especially in Russia( Reference Sõukand, Pieroni and Biró 15 , Reference Marsh, Hill and Ross 22 , Reference Dlusskaya, Jänsch and Schwab 48 , 49 ). In the past, it was also consumed in parts of Eastern Poland( Reference Arici and Daglioglu 41 , Reference Todorov, Botes and Guigas 47 ). In Estonia, kali, a beverage similar to kvass, was produced in conjunction with beer, from the grain surplus after the production of beer( Reference Sõukand, Pieroni and Biró 15 ).
Kvass is a sparkling, sweet or sour beverage with a rye bread flavour and golden-brown colour( Reference Sõukand, Pieroni and Biró 15 , Reference Marsh, Hill and Ross 22 , Reference Dlusskaya, Jänsch and Schwab 48 , 49 ), while mint kvass is slightly carbonated( 49 ). Mint kvass is served chilled and it is popular in Russia ‘fast food’ restaurants( 49 ). Kvass contains carbohydrates (mainly maltose, maltotriose, glucose and fructose), proteins and amino acids, lactic and acetic acid, ethanol, minerals and vitamins originating from the raw materials or from the microbial metabolic activity( Reference Dlusskaya, Jänsch and Schwab 48 ).
Two main kvass-making techniques exist, which use as raw material either stale sourdough bread or malt( Reference Dlusskaya, Jänsch and Schwab 48 ). In the first technique, the sugars needed for the yeast fermentation derive from the bread, while in the second, rye malt and rye flour (boiled with excess water) are the raw materials and gelatinised starch is cleaved by malt enzymes. In case the rye bread is not stale, it should be placed in the oven in order to be dried slowly( Reference Albuquerque, Costa and Sanches-Silva 42 , Reference Dlusskaya, Jänsch and Schwab 48 ). Before the addition of starter and sugar, the kvass batter is diluted in boiling water and clarified by sedimentation. Kvass southern preparation methods are baking and boiling( Reference Albuquerque, Costa and Sanches-Silva 42 ). The main stages of the preparation method of mint kvass are: preparation of raw materials, drying in an oven, boiling, cooling and straining, sugar addition and fermentation( 49 ). When made at home, a sourdough stock culture is used as a starter/inoculum for the fermentation. Kvass is produced on an industrialised scale, using starters and the final product is often pasteurised and supplemented with preservatives( Reference Sõukand, Pieroni and Biró 15 , Reference Marsh, Hill and Ross 22 , Reference Dlusskaya, Jänsch and Schwab 48 ). Kvass is very rich in microbiota consisting of viable yeasts and LAB( Reference Dlusskaya, Jänsch and Schwab 48 ). Its microbiota of fermentation consists of LAB (Lb. casei, Ln. mesenteroides) and yeasts (Saccharomyces cerevisiae), but the composition on a species level is variable, due to differences in fermentation techniques and feedstock( Reference Marsh, Hill and Ross 22 , Reference Dlusskaya, Jänsch and Schwab 48 ).
Traditional fermented non-alcoholic or low-alcoholic fruit-based beverages
Hardaliye
Hardaliye is a fruit-based NAFB (Table 3). It is made from red grape juice and crushed black mustard seeds, even though other ingredients, such as pomace and sour cherry leaves, can also be used( Reference Coskun and Arici 51 , Reference Aydoğdu, Yıldrırm and Halkman 52 ). Sometimes benzoic acid is added as a preservative (at the industrial scale)( Reference Kabak and Dobson 21 , Reference Arici and Coskun 53 ). Hardaliye originates from Thrace, in the European part of Turkey, where it is widely consumed( Reference Aydoğdu, Yıldrırm and Halkman 52 , Reference Arici and Coskun 53 ). Its colour varies depending on the grape varieties used and the production methods( Reference Güven and Aksoy 54 ). It has an acidic taste( Reference Coskun and Arici 51 , Reference Aydoğdu, Yıldrırm and Halkman 52 ).
Table 3 Examples of traditional fruit-based low-alcoholic and non-alcoholic fermented beverages consumed in European countries
LAB, lactic acid bacteria.
Hardaliye is mostly homemade following the traditional method( Reference Altay, Karbancıoglu-Güler and Daskaya-Dikmen 20 ). The ingredients are pressed and left to ferment for 5–10 d at room temperature( Reference Kabak and Dobson 21 , Reference Marsh, Hill and Ross 22 ). The microbial population of hardaliye has been reported to be mainly composed of lactobacilli and unknown fungal species( Reference Marsh, Hill and Ross 22 ). Bacterial species which have been identified in naturally fermented hardaliye samples include: Lb. paracasei subsp. paracasei, Lb. casei subsp. pseudoplantarum, Lb. brevis, Lb. pontis, Lb. acetotoleran, Lb. sanfransisco and Lb. vaccinostercus ( Reference Arici and Coskun 53 ).
Gilaburu juice
Gilaburu juice is a traditional NAFB( Reference Yilmaztekin and Sislioglu 55 , Reference Sagdic, Ozturk and Yapar 56 ). The basic ingredients for the fermentation are European cranberry bush (Viburnum opulus L.) and water (Table 3). European cranberry bush, known as gilaburu in Turkey, is a red-coloured fruit with a special astringent taste, grown mainly around Kayseri city in Turkey. Occasionally, sugar is added to avoid the astringent taste. Gilaburu juice is rich in acetic acid( Reference Yilmaztekin and Sislioglu 55 ). It originates from the Kayseri province, in the central Anatolia of Turkey( Reference Yilmaztekin and Sislioglu 55 , Reference Sagdic, Ozturk and Yapar 56 ).
For the preparation of the beverage, the fruits are left in water in a dark place and at room temperature for about 3–4 months to ferment( Reference Yilmaztekin and Sislioglu 55 , Reference Sonmez, Alizadeh and Öztürk 57 ). Several LAB species have been identified, including mainly lactobacilli, in the fermenting microbiota, such as Lb. plantarum, Lb. casei, Lb. brevis, Lb. hordei, Lb. paraplantarum, Lb. coryniformis, Lb. buchneri, Lb. parabuchneri, Lb. pantheris and Lb. harbinensis, along with but also Leuconostoc, for example, Ln. mesenteroides, Ln. pseudomesenteroides ( Reference Sagdic, Ozturk and Yapar 56 ).
Traditional fermented non-alcoholic or low-alcoholic vegetable-based beverages
Sauerkraut juice
Sauerkraut juice or Kraut juice is the juice produced from white cabbage fermentation( 58 ) (Table 4). Sauerkraut juice is made from cabbage and salt, same as Sauerkraut (fermented cabbage) is( Reference Albuquerque, Costa and Sanches-Silva 42 ). Fermented cabbage juice is widely consumed in Germany (Sauerkrautsaft), Ukraine, Romania (moare), Serbia (rasol) and other regions in the Black Sea( Reference Albuquerque, Costa and Sanches-Silva 42 , Reference Costa, Albuquerque and Sanches-Silva 50 ). According to the common method of production, the cabbage is fermented and then the juice is pressed out. Typically, the final product contains a lot of salt. It has been shown that sauerkraut and sauerkraut juice could be prepared with a very low Na concentration as well as, with a low total mineral salt content. The sauerkraut juice, which is fermented with 0·5 % mineral salt is considered to have the best taste( Reference Karovičová and Kohajdová 59 ). The natural fermenting microbiota includes mainly LAB, such as Ln. mesenteroides, Lb. brevis, Lb. sakei and Lb. plantarum ( Reference Tamang, Watanabe and Holzapfel 35 , 58 , Reference Karovičová and Kohajdová 59 ).
Table 4 Examples of traditional vegetable-based low-alcoholic and non-alcoholic fermented beverages consumed in European countries
LAB, lactic acid bacteria.
Şalgam juice
Salgam (also spelled Shalgam or Şalgam) juice is a NAFB (Table 4). It is made from black or purple carrots (Daucus carota), turnips (Brassica rapa), bulgur (broken wheat) flour, sourdough, salt and water( Reference Turker, Aksay and Ekiz 60 ). In India, a similar product, kanji, is produced via the natural fermentation of carrots and the addition of salt, chilies and crushed mustard. Both products owe their colour to the anthocyanins present in the black carrot( Reference Kabak and Dobson 21 ). Salgam comes originally from the Cukurova province of Turkey but nowadays is consumed throughout the country( Reference Erten, Tanguler and Canbaş 61 ), especially in Adana, Hatay and Icel (the Mediterranean region of Turkey). Recently, it has become popular in urban centres, such as Istanbul, Ankara and Izmir, as well( Reference Tanguler and Erten 62 ). Salgam juice is typically produced on a home-scale; however, small quantities are being commercially produced( Reference Erten, Tanguler and Canbaş 61 ).
Salgam juice is red-coloured, cloudy and has a sour taste. It is rich in minerals (Ca, K and Fe), vitamins (A, C and B group vitamins), and has polyphenols content( Reference Erten, Tanguler and Canbaş 61 , Reference İncedayi, Uylaşer and Çopur 63 , Reference Baysal, Çam and Harsa 64 ). Typically, salgam juice accompanies meals( Reference Kabak and Dobson 21 ). The indigenous microbiota of naturally fermented salgam juice is mainly composed of LAB, with the predominant species being Lb. plantarum, Lb. brevis and Lb. paracasei subsp. paracasei ( Reference Tanguler and Erten 62 , Reference Arici 65 ). Yeasts, such as S. cerevisie, have been reported to contribute to the fermentation process( Reference Baysal, Çam and Harsa 64 ).
Traditional fermented non-alcoholic or low-alcoholic herb, spice and aromatic plant-based beverages
Kombucha
Kombucha is one of the most popular LAFB in the world (Table 5). Black tea and white sugar are used for its production although green tea can also be used( Reference Reiss 66 ). The drink was originally popular in China, but nowadays is consumed worldwide, showing an increasing popularity as a traditional soft drink( Reference Marsh, Hill and Ross 22 , Reference Cvetković, Markov and Djurić 67 , Reference Blanc 68 ). Kombucha has a slightly sweet, carbonated, acidic taste resembling sparkling apple cider( Reference Cvetković, Markov and Djurić 67 , Reference Dufresne and Farnworth 69 , Reference Tamang and Kailasapathy 70 ). Traditionally, it was a homemade drink and the preservation and supply of the symbiotic colony of bacteria and yeast was included in the process( Reference Dufresne and Farnworth 69 ), but nowadays it is also commercially available( Reference Cvetković, Markov and Djurić 67 ).
Table 5 Examples of traditional herbs, spices and aromatic plant-based low-alcoholic and non-alcoholic fermented beverages consumed in European countries
LAB, lactic acid bacteria.
For the preparation, tea leaves are added to boiling water and left to infuse for 10 min. A small amount of sugar is then added in the hot tea and the preparation is left to cool. Tea fungus is added to the mixture, which is left to ferment for 1–8 weeks. After the end of the fermentation, the tea fungus is removed from the surface and kept in a small volume of fermented tea for future use( Reference Dufresne and Farnworth 69 ). Regarding the metabolites of the fermentation, the final product contains mainly acetic acid( Reference Cvetković, Markov and Djurić 67 , Reference Nguyen, Dong and Nguyen 71 ) but also gluconic and glucuronic acids, ethanol and glycerol( Reference Blanc 68 , Reference Liu, Hsu and Lee 72 ).
The microbiota of kombucha’s fermentation has been examined by many research groups, which concluded that both LAB and yeasts are present during the fermentation( Reference Tamang and Kailasapathy 70 ), while some have reported that acetic acid bacteria also take part in the fermentation process( Reference Marsh, Hill and Ross 22 , Reference Nguyen, Dong and Nguyen 71 ). Recently, different kombucha samples were analysed using high-throughput sequencing and five bacterial phyla were revealed: Actinobacteria, Bacteroidetes, Deinococcus-Thermus, Firmicutes and Proteobacteria. The most abundant were Proteobacteria and the dominant genus was Gluconacetobacter, while Acetobacter was traced in lower populations. The Firmicutes were represented mostly by the Lactobacillus genus and Lactococcus was found mainly in kombucha pellicles. The genera Leuconostoc, Enterococcus and Allobaculum were detected for the first time in kombucha samples. Actinobacteria were not found in all samples but Propionibacterium and Bifidobacterium strains were detected in early stages of kombucha fermentation, for the first time. Culture-dependent techniques do not permit the detection of micro-organisms living in extreme thermophilic conditions like Thermus spp. (Deinococcus-Thermus), which was detected in the same study. Regarding yeasts, Zygosaccharomyces was the dominant genus but also Pichia, Dekkera and Kazachstaniagenera were found in tea( Reference Marsh, O’Sullivan and Hill 73 ).
Ginger beer
Ginger beer, also known as ginger ale, is a LAFB( Reference Madden 74 , Reference Weisburger and Corner 75 ) (Table 5). There are many different recipes for the production of ginger beer; however, the basic ingredients used are ginger, lemon, sugar and yeast( Reference Madden 74 ). Other ingredients used to improve its taste are mainly sugar, cream of tartar, dried ale or bread yeast, juniper berries (Juniperus communis), liquorice (Glycyrrhiza glabra) and chili (Capsicum annuum)( Reference Madden 74 ). At first, ginger beer was homemade, but soon it became commercialised and nowadays is consumed worldwide( 49 , Reference Madden 74 – Reference Smith 76 ). It is a sparkling soft drink with acidic taste and due to its low alcoholic content, it has become popular among children( Reference Madden 74 ).
The production of ginger beer began in England in the mid-1700s( Reference Madden 74 ), while the first written recipes date from the early 19th century( 77 ). The micro-organisms responsible for the fermentation of ginger beer are LAB and yeasts( Reference Dookeran, Baccus-Taylor and Akingbala 78 ). In particular, strains of the following genera have been identified in ginger beer samples, as a result of industrial fermentation: Lactobacillus, Leuconostoc, Bacillus, Staphylococcus, Candida and Saccharomyces ( Reference Osuntogun and Aboaba 79 ).
Traditional fermented non-alcoholic or low-alcoholic sucrose-based beverages
Sima
Sima is a sucrose-based LAFB, consumed in Finland. The ingredients used for its preparation include water, lemon, raisins, white and brown sugar and dried ale or bread yeast. Sima is a fermented soft drink of sweet taste and murky appearance. Typically, it is used to mark special occasions, such as May Day celebrations( 49 ). Due to its low alcoholic content, it is suited for consumption by children. The preparation method consists of six stages, the preparation of raw materials, boiling, cooling, straining, sugar addition and fermentation( 49 ).
Water kefir
Water kefir, also known as sugar kefir or tibicos, is a sucrose-based LAFB. The main ingredients used for its production are water kefir grains (a symbiosis of bacteria and yeast contained within grains), a sucrose solution, dried fruits (most commonly figs) and lemon( Reference Laureys and De Vuyst 80 – Reference Marsh, O’Sullivan and Hill 82 ). The most prevalent theory as to the origin of water kefir claims that water kefir grains are formed as granules fermented from sap on the pads of the Opuntia cactus in Mexico, but the drink is nowadays consumed worldwide( Reference Marsh, Hill and Ross 22 ). Water kefir is mostly a homemade beverage, while the grains for its preparation are usually passed from household to household( Reference Marsh, O’Sullivan and Hill 82 ).
Fermentation of water kefir lasts for 1 or 2 d at room temperature and results in a cloudy, carbonated and straw-coloured drink( Reference Gulitz, Stadie and Wenning 81 ). The product is lightly carbonated and acidic( Reference Gulitz, Stadie and Wenning 81 , Reference Marsh, O’Sullivan and Hill 82 ). The micro-organisms responsible for water kefir fermentation are LAB, acetic acid bacteria and yeasts( Reference Laureys and De Vuyst 80 , Reference Franzetti, Galli and Pagani 83 ). Recently, two research groups published the microbiological analysis of water kefir samples, using high-throughput sequencing techniques( Reference Marsh, O’Sullivan and Hill 82 , Reference Gulitz, Stadie and Ehrmann 84 ). Interestingly, the microbiota analysis has given different results probably due to the different origin of the samples. In the samples from the UK, USA and Canada three bacterial phyla were identified: Actinobacteria, Firmicutes and Proteobacteria. Proteobacteria were predominant in the grains, while Firmicutes were more abundant in the fermentates. The Zymomonas genus was dominant in all the samples, with the next common being the Lactobacillus genus. Leuconostoc was traced, but lactococci were not found. Acetobacter and Gluconacetobacter were also present. Bifidobacteriaceae were identified in small amounts but they could not be identified to the genus level( Reference Marsh, O’Sullivan and Hill 82 ). Gulitz( Reference Gulitz, Stadie and Ehrmann 84 ), analysed water kefir samples from different regions of Germany and according to their results Lactobacillaceae were the most abundant bacteria, followed by Bifidobacteriaceae. Acetobacteriaceae were traced in all the samples but in low amounts. They focused on the bifidobacteria analysis and identified Bifidobacterium psychraerophilum as the main species, which was also isolated( Reference Gulitz, Stadie and Ehrmann 84 ). As for the yeasts, different species have been associated with water kefir natural fermentation. Specifically, Saccharomyces, Hanseniaspora/Kloeckera, Zygotorulaspora and Candida strains have been found in water kefir samples( Reference Neve and Heller 85 ), whereas other researchers report Dekkera spp. (D. anomola, D. bruxellensis), Hanseniaspora spp. (H. valbyensis, H. vineae), S. cerevisiae, Lachancea fermentati, Zygosaccharomyces subsp. (Z. lentus, Z. florentina) and Meyerozyma subsp. present in the beverage( Reference Marsh, Hill and Ross 22 , Reference Marsh, O’Sullivan and Hill 82 ).
Health benefits of traditional low-alcoholic and non-alcoholic fermented beverages
The notion that the consumption of traditional LAFB and NAFB is associated with health benefits is widespread; for example, kefir has a reputation for beneficial effects on gastrointestinal disorders( Reference Mayo, Ammor and Delgado 18 ). However, health claims are mostly based on personal experiences and testimonials of individuals who habitually drink these beverages while the experimental evidence is still fragmentary, as the ideal methodology for research, for example, randomised controlled clinical trials, is not easy to apply. Most of the studies which investigated traditional LAFB and NAFB and their impact on health have focused on two beverages, kefir and kombucha. Thus, the association between traditional LAFB and NAFB and health has not been scientifically proven yet. Nevertheless, as their alleged health-promoting properties are deeply rooted in the respective cultures, they deserve to be further examined via controlled clinical studies in other cultural origins and in current conditions of living.
Besides the nutrients of the raw unfermented ingredients, LAFB and NAFB also contain micro-organisms, as well as metabolites and protein breakdown products( Reference Ebringer, Ferenčík and Krajčovič 86 ). The primary metabolic actions of the starter cultures in food and beverage fermentations include their ability to predominantly ferment carbohydrates and, to a lesser degree, degrade proteins and fats in the raw material. This leads to the production of a broad range of metabolites, mainly organic acids (for example, lactic, acetic, formic, propionic), peptides, amino acids and NEFA, along with many volatile and non-volatile low-molecular-mass compounds, such as ketones and esters. Other metabolites, such as antimicrobial compounds (for example, carbon dioxide and ethanol as well as antimicrobial peptides and proteins known as bacteriocins), exopolysaccharides, enzymes (for example, amylases) and vitamins are also often produced. This way, starter cultures enhance the product’s shelf-life and microbial safety( Reference Leroy and De Vuyst 6 ).
In recent years, a special category of starter or adjunct micro-organisms, the so-called probiotics, have been recognised to be involved in food fermentations( Reference Khani, M Hosseini and Taheri 87 ). Probiotic foods and beverages are considered as health-promoting foods and belong to the so-called functional foods with large and expanding commercial interest. As presented in the above section, many traditional NAFB and LAFB are good sources of probiotics. Probiotics mainly belong to the LAB group and when taken up in adequate amounts confer a health benefit on the host( Reference Tamang, Shin and Jung 37 ). Even if it is not easy to declare health-promoting effects, probiotics have been implicated in the management of gastrointestinal tract diseases, alleviation of lactose intolerance, reduction of the risk for certain types of cancer, treatment of ulcerative colitis and Helicobacter pylori infection, whereas they have been suggested to exert antihypertensive and hypocholesterolic effects( Reference Khani, M Hosseini and Taheri 87 – Reference Takano 89 ). Some of the aforementioned effects are supported by clinical studies; however, issues such as the site and mode of action, viability, effectiveness after food handling and storage and the minimum quantity necessary to promote a health effect are still under examination( Reference Mercenier, Pavan and Pot 90 ). Attributed and evidence-based health benefits of the various categories of LAFB and NAFB are presented in the following sections.
Traditional fermented low-alcoholic and non-alcoholic milk-based beverages
Same as milk, fermented milk products are also good sources of proteins, lipids and carbohydrates; in addition, they contain bioactive compounds, most importantly immunoglobulins, bioactive peptides, hormones, cytokines and growth factors( Reference Neve and Heller 85 ). This complex mixture of substances influences many biological functions, such as the stimulation of cellular proliferation and gastrointestinal function and maturation in the postnatal state, contributing to the adaptation of the newborn child( Reference Neve and Heller 85 ). Fermented milks are also rich in exopolysaccharides, such as kefiran in kefir, which are considered to have a beneficial impact, especially as antioxidant, anti-tumour, antimicrobial and immunomodulating agents( Reference Tamang, Shin and Jung 37 , Reference Hugenholtz 91 ). Thus, the superiority of fermented against non-fermented milk stems from its microbiota and bioactive compounds.
Fermented dairy products help in the alleviation of lactose intolerance, not only because they have a reduced lactose content compared with milk, but also due to the secretion of bacterial lactase from LAB stains into the stomach and intestine( Reference Khani, M Hosseini and Taheri 87 ). In children with acute diarrhoea and carbohydrate malabsorption, the gastrointestinal diseases and, most importantly, the decreased duration of acute diarrhoea and stool frequency, were shown to be associated with the feeding of yoghurt, while the cessation of diarrhoea and weight gain of these children were similar to either yoghurt or milk feeding groups( Reference Boudraa, Benbouabdellah and Hachelaf 92 ). Fermented milk can also be valuable in complementary feeding, targeting the prevention of Fe-deficiency anaemia and also the prevention and shortening the length of gastrointestinal infections via the action of probiotics. Furthermore, fermented milk can contribute to the prevention of malnutrition in young children living in regions with limited access to animal-origin foods, high prevalence of parasites, low hygiene levels in food handling and unsafe drinkable water( Reference Branca and Rossi 93 , Reference Solis, Samartin and Gomez 94 ).
Natural fermented milks have been examined for a number of health-promoting effects. Kefir in particular has been accredited with the ability to normalise the intestinal microbiota and reduce the symptoms of lactose intolerance( Reference Battock and Azam-Ali 9 , Reference Mayo, Ammor and Delgado 18 , Reference Kabak and Dobson 21 , Reference Lopitz-Otsoa, Rementeria and Elguezabal 24 , Reference Özdestan and Üren 25 , Reference de Oliveira Leite, Miguel and Peixoto 95 ). With regard to gastrointestinal diseases, in Russia, kefir has been routinely administrated for the treatment of peptic ulcers( Reference Farnworth and Mainville 96 ). The administration of kefir in an animal model was associated with a significantly increased number of LAB and reduced number of enterobacteria and clostridia( Reference Marquina, Santos and Corpas 97 ). Kefir’s antimicrobial activity against a wide variety of Gram-positive, Gram-negative bacteria and fungi, some of them being considered as foodborne pathogens or food spoilage micro-organisms, is related to compounds such as lactic acid, carbon dioxide, volatile acids and bacteriocins( Reference Mayo, Ammor and Delgado 18 , Reference Altay, Karbancıoglu-Güler and Daskaya-Dikmen 20 ). Similarly, ayran, a salt-containing yoghurt drink, is a vehicle of viable LAB such as Lactobacillus delbrueckii subsp. bulgaricus and S. thermophilus ( Reference Morelli 98 ). Yoghurt’s potential to alleviate symptoms of lactose intolerance has been well documented and is considered to be a species-related trait of LAB( Reference Tamang, Shin and Jung 37 ). In men with chronic malabsorption, the consumption of a fermented dairy product (yoghurt) was associated with alleviated symptoms and decreased breath hydrogen status( Reference Rizkalla, Luo and Kabir 99 ). Other strain-specific health properties of traditional yoghurt living cultures are the immunomodulatory impact of a L. bulgaricus specific strain supported by both in vitro and in vivo studies( Reference Makino, Ikegami and Kume 100 ). The endproducts of kefir fermentation, namely the peptides derived from a mild proteolysis of the milk caseins, have been found to be associated with immunomodulating activity on the gut and stimulation of the immune system in mice( Reference Vinderola, Perdigón and Duarte 101 ). For the case of antibiotic associated diarrhoea, however, a clinical trial, the Kefir (MILK) Study, failed to show a positive impact on its prevention when kefir was administered( Reference Merenstein, Foster and D’Amico 102 ).
Besides the effects related to the normalisation of the intestinal microbiota, natural fermented milks have been examined for their potential to protect against cardiovascular risk factors( Reference Tamang, Shin and Jung 37 , Reference Tamang and Kailasapathy 70 ). In an animal study in hypercholesterolaemic rats, the oral administration of kefir resulted in reductions of VLDL-cholesterol, LDL-cholesterol and TAG levels and increased HDL-cholesterol levels( Reference Angelis-Pereira, Barcelos Mde and Sousa 103 ). Similar results emerged from another study with cholesterol-fed hamsters, in which kefir was associated with lowered levels of TAG, total cholesterol, cholesterol accumulation in the liver and non-HDL fraction( Reference Liu, Wang and Chen 104 ). Furthermore, kefiran, the exopolysaccharide of kefir, has been associated with the prevention of atherosclerosis in rabbits fed with a high-cholesterol diet( Reference Uchida, Ishii and Inoue 105 ). On the contrary, a clinical study with mildly hypercholesterolaemic men, who consumed kefir, did not result in low levels of plasma lipids( Reference St-Onge, Farnworth and Savard 106 ). Apart from natural fermented milks, functional fermented milks with strains isolated from naturally fermented dairy products have also been used in order to improve serum lipid levels( Reference Hugenholtz 91 ). Recently, it has been shown that the addition of a Lactobacillus helveticus strain isolated from fermented cows’ milk in the diet of hypercholesterolaemic mice was associated with the reduction of the serum total cholesterol level, while a significant decrease in the LDL-cholesterol level was also observed( Reference Damodharan, Palaniyandi and Yang 107 ).
Furthermore, an antihypertensive effect of fermented milks has also been shown in vivo, in both human studies and animal models (rats); this effect is believed to be mediated by the production of angiotensin-converting enzyme (ACE)-inhibitory peptides (antihypertensive bioactive peptides) released during fermentation( Reference Domínguez, Cruz and Márquez 108 ). Beltrán-Barrientos et al. ( Reference Beltrán-Barrientos, Hernández-Mendoza and Torres-Llanez 109 ) reviewed seven different clinical trials that assessed the effect of fermented milk consumption on blood pressure and concluded that significant decreases of blood pressure were noticed and that they can be attributed to the use of Lactobacillus helveticus strains( Reference Beltrán-Barrientos, Hernández-Mendoza and Torres-Llanez 109 ). On the contrary, a clinical trial among type 2 diabetes patients who were randomly assigned to receive daily a fermented milk with L. helveticus for 12 weeks failed to show any significant reduction in blood pressure after the consumption of this ‘functional’ milk( Reference Hove, Brøns and Faerch 110 ).
Some experimental evidence exists for other purported health benefits of milk-based NAFB and LAFB, such as their impact on obesity. An in vitro study has shown that kefir could act as a regulator for obesity, due to the inhibition of the adipocyte differentiation( Reference Ho, Choi and Lim 111 ). Another study using genetically obese mice (ob/ob) suggested that oral administration of kefir was associated with the suspension of lipogenesis and, thus, protection against non-alcoholic fatty liver disease( Reference Chen, Tung and Tsai 112 ). With regard to yoghurt’s effect to prevent weight gain, the Seguimiento University of Navarra (SUN) cohort study has shown that there is an inverse association between its consumption and the incidence of overweight and obesity in adults, especially when yoghurt is part of a healthy dietary regimen and is accompanied by high fruit consumption( Reference Martinez-Gonzalez, Sayon-Orea and Ruiz-Canela 113 ). Furthermore, an observational, cross-sectional study that was conducted among adolescents in eight European cities (HELENA) showed that consumption of dairy products, including milk, yoghurt and fermented milks, was inversely associated with total and abdominal excess body fat( Reference Moreno, Bel-Serrat and Santaliestra-Pasías 114 ).
The impact of the consumption of fermented milks on bone metabolism and bone mineral density has also been investigated. In a double-blind cross-over study, the consumption of fermented milk with Lactobacillus helveticus by twenty postmenopausal women had a positive acute effect on their Ca metabolism, compared with milk consumption and with juice containing peptides formed by the same strain( Reference Narva, Nevala and Poussa 115 ). A recent clinical trial measured the effects of kefir supplemented with calcium bicarbonate on bone mineral density and metabolism in forty osteoporotic men and women for 6 months, and compared them with unfermented raw milk also supplemented with calcium bicarbonate. The kefir consumption was associated with improved bone mineral density and with significantly increased serum parathyroid hormone( Reference Tu, Chen and Tung 116 ). In a study with an ovariectomised rat model having postmenopausal osteoporosis, it was observed that a 12-week treatment with kefir could be beneficial to the prevention or treatment of osteoporosis( Reference Chen, Tung and Chuang 117 ).
Another health effect that has been attributed to fermented milk products is their antioxidant capacity. In this respect, an in vitro study using human colon cells has found that both kefir and ayran have an antioxidant potential that may prevent DNA damage( Reference Grishina, Kulikova and Alieva 118 ). When administered in diabetic rats, kefir was associated with reduced oxidative stress, and improved renal function, one of the main diabetic complications( Reference Punaro, Maciel and Rodrigues 119 ).
From the above it can be concluded that the published evidence on fermented milks provides substantial grounds for supporting the potential of these beverages to modulate gut microbiota and, thus, improve the gastrointestinal function. The evidence on other health benefits, such as the impact on CVD risk factors and osteoporosis, is weak and therefore these claims require further evaluation.
Traditional fermented non-alcoholic or low-alcoholic cereal-based beverages
The impact of the consumption of traditional cereal-based LAFB and NAFB on health has also received attention. These beverages are sources of nutrients and other substances, such as minerals, vitamins, fibres, flavonoids and phenolic compounds, which could protect from oxidative stress, inflammation, hyperglycaemia and tumorigenesis( Reference Taylor and Duodu 120 ). Moreover, their microbial content and metabolites may also contribute to their health-promoting effects. In particular, boza has been found to have probiotic properties( Reference Altay, Karbancıoglu-Güler and Daskaya-Dikmen 20 , Reference Kabak and Dobson 21 , Reference Gotcheva, Pandiella and Angelov 43 – Reference Todorov, Botes and Guigas 47 ), while the various metabolites of LAB that it contains, such as lactic acid, confer antimicrobial properties and positive effects on digestion and intestinal microbiota( Reference Arici and Daglioglu 41 , Reference Yeğin and Üren 45 ).
Traditional fermented non-alcoholic or low-alcoholic fruit-based beverages
The data concerning the potential health effects of traditional fruit-based LAFB and NAFB are scarce. Recent research has found that the European cranberry bush (Viburnum opulus L.), the main ingredient of gilaburu juice, is rich in antioxidants and has antimicrobial properties( Reference Sagdic, Ozturk and Yapar 56 , Reference Levent Altun, Saltan Çitoğlu and Sever Yilmaz 121 , Reference Andreeva, Komarova and Yusubov 122 ). Furthermore, its juice may be chemopreventive at the early stages of colon cancer, as reported from the treatment of mice after 1,2 dimethylhydrazine (DMH)-induced colon cancer( Reference Ulger, Ertekin and Karaca 123 ). Furthermore, because it contains several LAB species, gilaburu juice is deemed to have a probiotic potential( Reference Yilmaztekin and Sislioglu 55 , Reference Sagdic, Ozturk and Yapar 56 ). According to the results of a randomised controlled clinical trial, hardaliye exhibits antioxidant activity( Reference Amoutzopoulos, Löker and Samur 124 ).
Traditional fermented non-alcoholic or low-alcoholic vegetable-based beverages
Among the various vegetable-based LAFB and NAFB, data exist only for sauerkraut juice. More specifically, research has been conducted to test its role in helping digestion, normalising the function of the stomach and gut, as well as in providing antimicrobial, antioxidant and anti-tumour effects( Reference Tamang, Shin and Jung 37 ). The health-promoting components of sauerkraut juice and its impact on health have been studied in a few in vitro and in vivo animal studies( 58 ). An in vitro study has shown that sauerkraut juice, which was produced via short and prolonged fermentation by LAB, had a more pronounced antioxidant effect compared with non-fermented cabbage( Reference Kusznierewicz, Śmiechowska and Bartoszek 125 ). Also, an animal study has indicated that the chemoprotective properties of sauerkraut juice may be attributed to the activation of the detoxifying enzymes( Reference Krajka-Kuźniak, Szaefer and Bartoszek 126 ). Another animal study which examined rat liver and kidneys has shown that sauerkraut juices may have anticarcinogenic and chemopreventive effects via the inactivation of carcinogens/xenobiotics( Reference Szaefer, Krajka‐Kuźniak and Bartoszek 127 ). However, the above evidence needs to be enriched with additional data, in order for the health claims about sauerkraut juice to become substantiated.
Traditional fermented non-alcoholic or low-alcoholic herb, spice and aromatic plant-based beverages
The proposed health effects of kombucha, a fermented sweetened tea, have been attributed first to the protective impact of tea itself, and second to the products formed during the fermentation, namely its content in glucuronic acid, acetic acid, polyphenols, phenols and B-complex vitamins, including folic acid( Reference Dufresne and Farnworth 69 , Reference Wang, Ji and Wu 128 ). The acid content of kombucha resulting in reduced pH, in conjunction with antimicrobial substances produced by the bacteria and the alcohol (although it is not always detected), may have an antimicrobial and curative potential( Reference Marsh, Hill and Ross 22 ). Glucuronic acid, an endproduct of kombucha’s fermentation, is thought to be one of the key components for its proposed health effect on liver and gastrointestinal function and also on immune stimulation( Reference Wang, Ji and Wu 128 ). d-Saccharic acid-1,4-lactone (DLS), which is produced from Gluconacetobacter sp. A4 (a micro-organism found in kombucha), may facilitate glucuronic acid to exert detoxifying, antioxidant and anti-tumour properties. Wang et al. have found that the hepatoprotective properties of kombucha are attributed to the presence of DLS in it and also that Gluconacetobacter sp. A4 is the key functional strain responsible for these protective effects( Reference Wang, Ji and Wu 128 ).
Other recent in vitro and in vivo experimental studies, mainly in mice and rats, have also reported that kombucha may exert health prophylactic and recovery effects, through immune stimulation, detoxification, antimicrobial activity, as well as antioxidation( Reference Dufresne and Farnworth 69 , Reference Angelis-Pereira, Barcelos Mde and Sousa 103 , Reference Greenwalt, Steinkraus and Ledford 129 , Reference Vīna, Semjonovs and Linde 130 ). One study has shown that kombucha was more efficient to revert the CCl4-induced hepatotoxicity in rats when compared both with black tea and with enzyme-processed tea with tea fungus; this was attributed to the antioxidants produced during the fermentation process( Reference Murugesan, Sathishkumar and Jayabalan 131 ). Furthermore, the antioxidant capacity of polyphenols, mainly flavonols and catechins found in kombucha, may prevent the development and inhibit the progression of many chronic human diseases, including cancer, CVD, diabetes and neurodegenerative diseases. The availability of B-complex vitamins and especially folic acid in kombucha may also contribute to the normal central nervous system function at all ages and help towards the prevention of disorders related to the central nervous system( Reference Dufresne and Farnworth 69 , Reference Angelis-Pereira, Barcelos Mde and Sousa 103 , Reference Greenwalt, Steinkraus and Ledford 129 , Reference Vīna, Semjonovs and Linde 130 ). As the majority of the data on kombucha’s effects arise from in vitro and in vivo (animal) studies, human clinical studies are needed in order to clarify its health benefits and the mechanisms of action.
Apart from kombucha, advocates of ginger beer have attributed health benefits to this beverage, especially counterirritant properties and a capacity to alleviate the symptoms of an upset stomach( Reference Smith 76 , 77 ). However, its impact on health has not been evaluated yet.
Traditional fermented non-alcoholic or low-alcoholic sucrose-based beverages
The evidence on the two sucrose-based LAFB and NAFB, water kefir and sima, is very fragmentary and limited to water kefir. Water kefir is believed to be a health-promoting beverage. It contains strains from species, such as lactobacilli and bifidobacteria, which are generally considered to have probiotic properties( Reference Gulitz, Stadie and Ehrmann 84 ). To date, however, the research on water kefir is very limited and its health benefits have yet to be investigated( Reference Marsh, O’Sullivan and Hill 82 ). Evidence on the health-promoting effects of sima, another traditional sucrose-based LAFB, is completely missing.
Potential health risks of traditional non-alcoholic or low-alcoholic fermented beverages
Even though the consumption of non- or low-alcoholic fermented beverages is generally considered safe, there are some aspects arising from toxic compounds traced in fermented milks and cereal-based fermented products. The main substances found with toxic activity, depending on their concentration, are biogenic amines, such as tyramine, putrescine, cadaverine, spermidine and tyramine. They are produced by LAB of Enterococcus, Lactobacillus, Leuconostoc and other genera, via the decarboxylation of amino acids. The consumption of foods containing biogenic amines might represent a health risk for patients with neurodegenerative diseases treated with monoamine oxidase inhibitor drugs( Reference Fernández, Hudson and Korpela 132 ).
In a survey conducted in kefir samples from different producers, a number of biogenic amines were traced. Total amines varied from 2·4 to 35·2 mg/l, and tyramine was the predominant, traced in almost all the samples. Putrescine, cadaverine and spermidine were also detected. Based on the current knowledge, their concentrations in the examined samples do not seem to be of great concern( Reference Özdestan and Üren 25 ). In another study searching biogenic amines in boza samples from different producers, putrescine, spermidine and tyramine were found in all samples. Total biogenic amines concentration varied between 25 and 69 mg/kg; tyramine was the dominant amine( Reference Yeğin and Üren 45 ). As there are no data regarding the association between the consumption of these beverages and toxicity, more experimental evidence is required. Furthermore, the attributed toxic activity of biogenic amines poses the need for regulatory authorities to adequately standardise their concentration limits in traditional non- or low-alcoholic fermented beverages.
For kombucha, there are a few reports associating daily consumption with stomach upset, or allergic reactions. The mechanism connecting the causality of kombucha consumption to these adverse effects has not been yet proposed, but the cessation of its intake ameliorated the health status of these patients( Reference Frank 133 , Reference Srinivasan, Smolinske and Greenbaum 134 ). A case of cutaneous anthrax has also been associated with unhygienic kombucha tea exposure in Iran( Reference Sadjadi 135 ). Some health disorders, such as hepatotoxicity and severe metabolic acidosis, have been linked to kombucha consumption, possibly after chronic or excessive consumption( Reference Greenwalt, Steinkraus and Ledford 129 , Reference Hartmann, Burleson and Holmes 136 ). Recently, a case of hepatotoxicity related to kombucha consumption was published( Reference Gedela, Potu and Gali 137 ). Finally, a pilot study in mice reported some adverse effects, such as splenomegaly and hepatomegaly, after chronic kombucha injection( Reference Hartmann, Burleson and Holmes 136 ).
Regarding kvass, a cereal-based beverage popular in Russia and other countries, concerns have been published for its possible contribution to chronic alcoholism in the former Soviet Union. Kvass content of alcohol is generally below 1·5 %, but due to its low price has been massively consumed even by adolescents and children( Reference Jargin 138 ).
Commercialisation of indigenous non-alcoholic or low-alcoholic fermented beverages
Traditional non-alcoholic or low-alcoholic fermented beverages and their place in the market
Non- and low-alcoholic fermented beverages have gained consumers’ acceptance worldwide. Their demand stems from long-rooted established practices, as well as their sensorial properties. In the past, NAFB and LAFB were found mainly in rural markets, such as small- and large-scale farms and local village markets, but recently have become available in urban markets as well. A variety of LAFB and NAFB are commercially available in many cities( Reference Perricone, Bevilacqua and Corbo 139 ) (Tables 1, 2, 3, 4 and 5). Most of them are dairy products, for instance kefir ( Reference Marshall and Mejia 140 ). Examples of other than dairy NAFB, which are commercially available in European markets, are kvass and kombucha.
In countries where a standardised production for NAFB and LAFB exists, their consumption has exhibited an increase over the past decades. Dairy fermented beverages, with fermented milks and yoghurt-like drinks being the most representative, comprise the majority of the health-promoting fermented beverages. Dairy NAFB and LAFB are widely consumed in northern European countries, such as Denmark, Sweden and Finland( Reference Ozen, Pons and Tur 141 ) (Fig. 1), but are less consumed in other countries such as France, German, Spain and the UK( Reference Perricone, Bevilacqua and Corbo 139 ). Based on a series of studies focusing on the level of consumption of commercially produced fermented milk products in different countries, Finland had the highest level, with 91·6% of the participants reported consuming sour milk( Reference Marsh, Hill and Ross 22 , Reference Lahti-Koski, Pietinen and Heliövaara 142 ). Thus, the implementation of standards in the manufacturing of traditional NAFB and LAFB not only ensures the identity and quality of these products, but also helps in promoting their consumption in the general population.
Fig. 1 Annual per capita consumption of all fermented milks only in selected countries in Europe. Data were taken from Saxelin (2008)( Reference Madhu, Shiva Prakash and Neetu 166 ).
Innovations and perspectives of traditional non-alcoholic or low-alcoholic fermented beverages
Over the last decade, an increasing demand for health-promoting foods and beverages has been reported in many parts of the world( Reference Perricone, Bevilacqua and Corbo 139 ). This resulted in the expansion of ‘functional’ foods throughout the market, with a wide range of products, including beverages. Generally, there is no unanimously accepted international definition of ‘functional’ foods. From a science-based view, the European Commission Concerted Action on Functional Food Science in Europe (FuFoSE) describes a food as functional ‘if it is satisfactorily demonstrated to affect beneficially one or more target functions in the body, beyond adequate nutritional effects, in a way that is relevant to either an improved state of health and well-being and/or reduction of risk of disease’. It also states that ‘“functional” foods must remain foods and they must demonstrate their effects in amounts that can normally be expected to be consumed in the diet: they are not pills or capsules but part of a normal food pattern’( 143 ). This prerequisite represents a challenge when attempting to formulate legislations for regulating the market of functional foods( Reference Perricone, Bevilacqua and Corbo 139 ).
Dairy foods are estimated to account for almost 43 % of the functional foods market, the largest proportion of which is comprised of fermented products( Reference Özer and Kirmaci 144 ). The majority of fermented milks and yoghurt-like drinks fall within the category of probiotic beverages, the largest proportion of the functional food market( Reference Marsh, Hill and Ross 22 , Reference Perricone, Bevilacqua and Corbo 139 ). These beverages often contain strains of Lactobacillus spp. and Bifidobacterium spp., as well as other species. In their novel versions, Lb. acidophilus, Lb. rhamnosus, Lb. casei and B. bifidum are the most commonly added probiotics( Reference Perricone, Bevilacqua and Corbo 139 , Reference Özer and Kirmaci 144 , Reference Maukonen, Alakomi and Nohynek 145 ), while peptides, phytosterol, minerals and milk whey are the most commonly added bioactive compounds (for examples, see Table 6). In some cases, species of Saccharomyces and Candida may be added in commercially prepared fermented milks( Reference Gadaga, Mutukumira and Narvhus 146 ), but only Saccharomyces boulardii is considered as a yeast with probiotic properties. More recently, the production of probiotic fermented beverages from whey has received much attention( Reference Luana, Rossana and Curiel 147 ). A representative example of a fermented whey-based drink is Gefilus® (Valio Ltd) (Table 6). Whey is an endproduct of cheese manufacturing (a fermentation process), which retains almost half of the milk nutrients and is low in fat (0·36 %). A fermented whey-based drink can be produced by the addition of LAB, such as Streptococcus and Lactobacillus, on whey. These probiotic bacteria can survive and ferment whey( Reference Drgalic, Tratnik and Bozanic 148 ). Furthermore, it has been shown that the addition of starter cultures, such as kefir grains, can also result in the production of a fermented whey-based beverage( Reference Luana, Rossana and Curiel 147 ).
Table 6 Examples of commercially available functional low-alcoholic or non-alcoholic fermented beverages in European countries( Reference Perricone, Bevilacqua and Corbo 139 , Reference Özer and Kirmaci 144 , Reference Maukonen, Alakomi and Nohynek 145 )
The prospect of manufacturing non-dairy fermented beverages is currently very appealing, mostly as an alternative way to traditional dairy-based fermented beverages for delivering probiotics. Non-dairy beverages containing probiotic strains have recently been launched in the European market. Made of fruits, vegetables and cereals, these beverages are suitable for individuals allergic to milk, hypercholesterolaemics as well as for vegans, while they are good sources of antioxidants, fibres, vitamins and minerals( Reference Prado, Parada and Pandey 46 ). At the same time, they are free from substances found in dairy products, such as pesticides, oestrogen and insulin-like growth factor I (IGF-I) which might be responsible for a negative association between dairy products and health problems( Reference Perricone, Bevilacqua and Corbo 139 ). In particular, cereals serve as alternative substrates for the industrial production of non-dairy fermented beverages which contain probiotic and prebiotic ingredients( Reference Drgalic, Tratnik and Bozanic 148 ). Proviva® (Skane Dairy) was the first non-dairy fermented probiotic beverage, made of oatmeal gruel with the addition of LAB( Reference Prado, Parada and Pandey 46 ) (Table 6).
Ongoing research for developing new formulas for dairy and non-dairy LABF and NAFB products results in an expansion of the types available, beyond the traditional ones( Reference Prado, Parada and Pandey 46 ). Further evidence, which will substantiate their preventive or/and therapeutic health benefits, mode of action, optimal intake, selection of specific strains for a targeted outcome and mode of delivery, is needed. Also, information regarding the viability, metabolic activity and thus efficacy of probiotic bacteria in a beverage till the end of its shelf-life has to be considered. New product development requires detailed knowledge of the products’ details as well as the customers’ needs and behaviour( Reference Heenan, Adams and Hosken 149 , Reference Yoon, Woodams and Hang 150 ).
Discussion
LAFB and NAFB are important constituents of the human diet all around the world. Their value stems from their cultural significance, as their production has been interwoven with ecosystems and social structures of local communities( Reference Yoon, Woodams and Hang 150 , Reference Shiby and Mishra 151 ). In Europe, LAFB and NAFB produced from milk are the most abundant, with kefir, ayran and buttermilk being among the most representative ones. LAFB and NAFB made of cereals (such as boza and kvass), herbs, spices and aromatic plants (such as kombucha and ginger beer) as well as, sucrose-based (such as sima and water kefir) are also popular in some countries; LAFB and NAFB made of fruits (such as hardaliye and gilaburu juice) and vegetables (such as sauerkraut juice and salgam juice) are generally less well known.
By applying the process of fermentation, the nutritional value of the substrates of fermentation, milk, fruit, cereals and vegetables, can be modified via a spontaneous biological enrichment with essential amino acids, vitamins and bioactive compounds( Reference Tamang and Kailasapathy 70 ). For example, in fermented milks, via the process of biological enrichment, most of the lactose is converted to lactate and proteins to free amino acids, both of which are readily absorbed, thus enhancing the digestibility of the product( Reference Campbell-Platt 152 ). However, although consumption of LAFB and NAFB has received attention, information on their nutrient content is generally lacking. Thus, compiling information on the composition and nutritional value of LAFB and NAFB is important in order to properly update( Reference Albuquerque, Costa and Sanches-Silva 42 , Reference Costa, Albuquerque and Sanches-Silva 50 ). Furthermore, this knowledge will allow government authorities to compile scientifically based regulation requirements, beverage industries to promote these beverages based on information, nutritionists and dietitians in dietary planning and consultation, and finally scientists in research designing and explaining study results. In addition, a robust knowledge of traditional LAFB and NAFB from European countries will assist in the promotion of regional biodiversity and sustainability.
LAFB and NAFB produced in European regions are usually from cows’ milk (Table 1). However, at a global level, non-cows’ milk has a growing importance in production, culture, economy and ecology( Reference Faye and Konuspayeva 153 ). Non-cows’ milk is widely produced and consumed in Asia and Africa (approximately 50% of the produced milk), mainly in emerging or developing countries and in remote areas( 154 ). In Europe the majority of the produced non-cows’ milk comes from sheep( Reference Faye and Konuspayeva 153 ). Several of the milk-based LAFB and NAFB presented in Table 1 can be made from types of milk other than cows’ milk, such as sheep’s (sour milk, skyr, prokish, prostokvasha, lyntyca, žinčica), camel (kefir), buffalo (sour milk) or goats’ milk (Bulgarian buttermilk). Thus, milk-based LAFB and NAFB may represent an opportunity in the direction of poverty alleviation and environmental sustainability by contributing to the increasing demand for food quantity and quality, especially in poor and underdeveloped countries.
In the past, alleged health effects had been sufficient for the consumption of LAFB and NAFB. Nowadays, their link to health benefits requires evaluation. Well-designed studies could investigate the impact that their consumption has on human health and elicit the role of their bioactive ingredients, type of microbes and their content and by-products of fermentation, as their health effects are probably the result of a synergistic process( Reference Marsh, Hill and Ross 22 , Reference Perricone, Bevilacqua and Corbo 139 , Reference Shiby and Mishra 151 , Reference Corbo, Bevilacqua and Petruzzi 155 ). Many factors perplex the implementation of clinical trials: constrains of time and money, the required adherence by the participants to consume the prescribed beverage and the selection of appropriate placebos (both for LAFB and NAFB and diet regimen). However, the need for strict and standardised guidelines in designing and conducting experimental studies is necessary.
Generally, LAFB and NAFB are an under-researched group of foods. The great diversity observed in traditional LAFB and NAFB can be attributed to several factors, such as utilisation of different raw materials, variations in natural microbiota and fermentation conditions, and production methods applied( Reference Altay, Karbancıoglu-Güler and Daskaya-Dikmen 20 ). Our understanding would be facilitated by establishing a consensus with respect to the specification of the natural microbiota, description of these particular micro-organisms that are essential for fermentation, as well as their contribution, either as a consortium or as a single strain to the final composition of each beverage( Reference Marsh, Hill and Ross 22 ). Currently, the formulation of health drinks that are based on traditional LAFB and NAFB represent a challenging opportunity for the beverage industry.
Most of the LAFB and NAFB presented here have been only recently become available in the market. Thus, in order for the scientific and commercial food standards to be met, there is a need for improving their microbial and sensorial properties. The design and production of a second-generation LAFB and NAFB require the following actions: (1) the identification, quantification and standardisation of promising bioactive compounds; (2) the fingerprinting and characterisation of the indigenous microbiota of the artisanal products; (3) the selection of starters able to produce bioactive compounds; (4) the selection of strains with functional properties to enhance the health-promoting properties of traditional LAFB and NAFB; (5) the investigation of bioavailability and metabolism of ingredients with health-promoting potential; (6) the study of safety aspects related to the consumption of beverages with enhanced nutritional effects; and (7) the formulation of value-added products based on traditional LAFB and NAFB( Reference Altay, Karbancıoglu-Güler and Daskaya-Dikmen 20 , Reference Corbo, Bevilacqua and Petruzzi 155 ). These developing actions in the health-promoting beverage market need to rely on a collaborative effort between industry partners and academia. This way, clinical trials and solid evidence will guarantee the production of LAFB and NAFB with enhanced nutritional effects and justified health claims( Reference Khan, Grigor and Winger 156 ).
However, many of the fermented foods are still produced in the traditional manner, i.e. either by natural spontaneous fermentations or by employing the back-slopping method( Reference Prajapati and Nair 2 , Reference Fondén, Leporanta and Svensson 19 , Reference Tamang and Kailasapathy 70 , Reference Silk, Guo and Haenlein 157 ). Back-slopping results in a higher initial number of microbiota present in the raw material itself. The specific microbiota involved in the production of any particular LAFB/NAFB varies markedly from region to region, and even among households within small geographical regions. Furthermore, taking into consideration the existing variability in the processing parameters, which are also being employed between the different fermentation regimens and geographical regions, one may conclude that the achievement of a uniform LAFB/NAFB is an extremely difficult task. The above indicate that further research is needed in order to determine the microbiological and biochemical features of the traditional LAFB and NAFB in each European country. As industrialisation and urbanisation are currently the norm for European societies, there is a need for large-scale production that will result in traditional fermented beverages of a consistently high quality and safety( Reference Haard 158 ). The transition from a household procedure to an industrial-scale production is a complex process, which requires improvements in the process controls and overall quality and safety, such as the microbiological standpoint of the raw materials used in the production of these beverages.
Nowadays, many individuals in Western societies wish to follow a prudent lifestyle. LAFB and NAFB could be an integral part of this trend as they are linked to a traditional, sustainable food system while they may be capable of improving the nutritional status of many( Reference Vietmeyer 159 ). As the scientific knowledge on the role of probiotics expands, the need for alternative means of probiotic delivery also increases. The various dairy products are currently the vehicle of choice for delivering probiotics, and probiotics are responsible for the health benefits of many LAFB and NAFB. Furthermore, cheese whey is an inexpensive fermentation substrate with high nutritional value and some whey components, such as lactoferrin, growth factors and immunoglobulins are gaining commercial interest from the beverage industry( Reference Özer and Kirmaci 144 ). Thus, whey-based fermented beverages could constitute a larger part of European commercial beverages( Reference Jeličić, Božanić and Tratnik 160 , Reference Bulatović, Rakin and Mojović 161 ). In addition, LAFB and NAFB based on substrates other than milk, such as cereal and fruit juices, may also gain success among consumers. Cereal-based fermented drinks could be produced commercially in Europe and low-quality cereals could be used for the production of a highly nutritious product( Reference Gotcheva, Pandiella and Angelov 43 ).
The interest of consumers for the preparation and consumption of traditional LAFB and NAFB depends on their potential to have a good taste, to prevent disease and ensuring healthy lives and well-being at all ages( Reference Özer and Kirmaci 144 , Reference Corbo, Bevilacqua and Petruzzi 155 , Reference Koletzko, Aggett and Bindels 162 ). Full regulatory approval for claims requires the support of robust evidence( Reference Lalor and Wall 163 ). The European Food Safety Authority (EFSA), in accordance with Regulation (EC) no. 1924/2006, has also set scientific requirements for substantiating health claims related to gut and immune functions( 164 ). However, in the USA and Japan a health claim that is suggested but not supported by robust evidence is known as a qualified health claim and is permitted. This heterogeneity in the required evidence has resulted in diverse health claims being accepted by the competent agencies among different countries even in the same continent and eventually creates confusion to the consumer. Currently, only in a few European countries, for instance, Sweden, the UK and the Netherlands, existing regulations allow for an official approval of health claims( Reference Saxelin 165 ). Once the constitution of the new regulation from the European Union is in place, the use of unauthorised claims and promises will cease, thus ensuring the development of accurate claims in regards to the health benefits of products that target specific health conditions( Reference Marsh, Hill and Ross 22 , Reference Perricone, Bevilacqua and Corbo 139 , Reference Shiby and Mishra 151 , Reference Corbo, Bevilacqua and Petruzzi 155 ).
Conclusion
Historically, LAFB and NAFB produced and consumed by European populations have been important for their nutrition and well-being. The present review revealed a considerable variety of traditional LAFB and NAFB across Europe. Although the dietary significance for some of these beverages is well known, there is still much to be elicited, especially about those of marginal use. Moreover, the stock of local knowledge on the natural preparation processes of these traditional beverages appears to be at risk, because of the overreliance on commercially produced beverages which currently prevails, even in rural regions. This trend, combined with a decline in the transfer of knowledge and lack of documentation on the remaining traditional know-how concerning local microbiota, ingredients of fermentation and fermentation processes, has resulted in the marginalisation and, in some cases, even disappearance of homemade LAFB and NAFB today.
From a commercial perspective, an increasing interest in beverages with enhanced nutritional effects has made selected traditional milk-based LAFB and NAFB, such as kefir and ayran, widely available in many European markets. The health beverage market will benefit from the increase of knowledge on less widespread traditional LAFB and NAFB, such as those that are presented in this review. Based on the improvements in science and technology, as well as consumers’ increasing consciousness for healthy and sustainable diets, the future for LAFB and NAFB appears to be more promising than ever.
Acknowledgements
This present review was published as part of a PhD Thesis entitled ‘Non- and low- alcoholic fermented beverages. Their importance in nutrition and culture of European communities’, Harokopio University, Athens, Greece.
All authors contributed equally to the preparation of the present review.
The authors have no conflicts of interest.
