Functional Foods and Nondairy Probiotic Food Development: Trends, Concepts, and Products Daniel Granato, Gabriel F. Branco, Filomena Nazzaro, Adriano G. Cruz, and José A.F. Faria ABSTRACT: Recently, the focus of scientific investigations has moved from the primary role of food as the source of energy and body-forming substances to the more subtle action of biologically active food components on human health. There has been an explosion of consumer interest in the active role of food in the well-being and life prolongation, as well as in the prevention of initiation, promotion, and development of nontransmissible chronic diseases. As a result, a new term—functional food—was proposed. Among these foods, probiotics may exert positive effects on the composition of gut microbiota and overall health, and the market is increasing annually. An increased demand for nondairy probiotic products comes from vegetarianism, milk cholesterol content, and lactose intolerance. Therefore, the development of these products is a key research priority for food design and a challenge for both industry and science sectors. This article presents an overview of functional food development, emphasizing nondairy foods that contain probiotic bacteria strains. Functional Foods: Concepts and Market Strategies The primary role of diet is to provide enough nutrients to meet metabolic requirements, while giving the consumer a feeling of satisfaction and well-being. Recent knowledge, however, supports the hypothesis that, beyond meeting nutrition needs, diet may modulate various physiological functions and may play detrimental or beneficial roles in some diseases (Koletzko and others 1998). There is a threshold of a new frontier in nutrition sciences and indeed, at least in the Western world, concepts are expanding from the past emphasis on survival, hunger satisfaction, and preventing adverse effects to an emphasis on the use of foods to promote a well-being state, improving health, and reducing the risk of diseases. These concepts are particularly important in light of the increasing cost of health care, the steady increase MS 20091087 Submitted 11/1/2009, Accepted 1/12/2010 . Authors Granato and Branco are with Dept. of Food and Experimental Nutrition, Faculty of Pharmaceutical Sciences, Univ. of São Paulo, Av. Prof. Lineu Prestes, 580, B14, 05508-000, São Paulo, Brazil. Author Nazzaro is with Istituto di Scienze dell’Alimentazione, ISA-CNR, Via Roma, 64, 83100, Avellino, Italy. Authors Cruz and Faria are with Dept. of Food Technology, Faculty of Food Engineering, Univ. of Campinas, Campinas, Brazil. Direct inquiries to author Granato (E-mail: [email protected]). 292 in life expectancy, and the desire of older people for improved life quality (Roberfroid 2007). Given tight profit margins in the broader food industry, many manufacturers are seeking ways to create and increase value. This includes a large number of product types, including convenience, organic and “better for you” foods, as well as functional foods. Claiming health properties is a clear way to differentiate products and, in most cases, hike up prices and improve profit levels. Therefore, the functional food and beverage market has attracted a large number of standard food and drink companies. A survey conducted by Siegrist and others (2008) with 249 people in Switzerland showed that consumers are more inclined to buy functional foods with physiological health claims compared with psychological health claims. Health claims were most positively evaluated when attached to a product with a positive health image. Older consumers were more interested in functional foods than younger consumers. The rise of functional foods has occurred at the convergence of several critical factors, such as: awareness of personal health deterioration, led by busy lifestyles with poor choices of convenience foods and insufficient exercise; increased incidence of self-medication; increased level of information from health authorities and media on nutrition and the link between diet and health; scientific developments in nutrition research; and a COMPREHENSIVE REVIEWS IN FOOD SCIENCE AND FOOD SAFETY—Vol. 9, 2010 c R 2010 Institute of Food Technologists Functional foods . . . Mass market positioning Sensory appeal Effective communication of health benefits Health benefits linked to common complaint Focus on general wellbeing MARKET SUCCESS OF FUNCTIONAL FOODS Price and convenience Figure 1 --- Strategies for functional food success in the marketplace. Loyalty to brand Industrial management and quality control crowded and competitive food market, characterized by pressurized margins (Siró and others 2008). These factors have created a dynamic functional food and beverage market, offering good prospects for growth for well-positioned food and drink manufacturers. Between 1998 and 2003, global value sales increased by almost 60%, and by almost 40% in 2008 (Euromonitor 2009). The average North-American consumer spends approximately US$ 90 per year on functional foods and beverages, resulting in a market exceeding US$ 27 billion in 2007. In the year 2000, the world-wide market of functional foods generated US$ 33 billion, in 2005 this total was US$ 73.5 billion (Justfood 2006), and the market is estimated to reach US$ 167 billion after 2010, with a yearly growth potential of 10% (Research and Markets 2008). In Brazil, the sales of functional foods in 2007 reached US$ 500 thousand, corresponding to almost 1% of the total food sales; moreover, around 65% of the total Brazilian functional foods are probiotic products (Cruz and others 2007). In Japan, regarded as the birthplace of functional food, the market of these products is significant. In total, more than 1700 functional food products have been launched in Japan between 1988 and 1998 with an estimated turnover of around 14 billion US$ in 1999 (Menrad 2003). The European market for functional foods was estimated to be between 4 and 8 billion US$ in 2003 depending which foods are regarded as functional. This value has increased to around 15 billion US$ by 2006 (Kotilainen and others 2006). The current market share of functional food is still below 1% of the total food and drink market. Germany, France, the United Kingdom, and the Netherlands represent the most important countries within the functional food market in Europe (Makinen-Aakula 2006). Functional food market in 2006 represented approximately 17% of the total food market in Spain; moreover, the predicted value for 2020 is to be around 40% higher. More than 50% growth was reported between 2000 and 2005 (Monar 2007). The market was estimated to be 5 billion US$ in 2003 (Side 2006) and 5.73 billion US$ in 2006, while more than 500 products were labeled as FOSHU in 2005 (Side 2006; Fern 2007). Strong growth is occurring in many functional food categories, and some of the more dynamic areas include probiotic yogurts, plant sterol spreads, energy bars, functional waters, juices, desserts, and cheeses. In terms of therapeutic areas, key growth areas include cholesterol lowering, gut health, and bone mineralization products (Sanders 2003; Shah 2007). Gut health products are particularly important in Japan, but relatively underdeveloped in the United States, where fortification with fiber, calcium, and vitamins, along with energy-giving products, are more pronounced. The market for functional foods varies greatly across regions, with Asia/Australia being clearly dominant, due to the massive Japanese market, while Eastern Europe and Africa remain very underdeveloped (Euromonitor 2009). In Brazil, the market for functional food, although underdeveloped, has begun to grow due to a high input of industries that have created new palatable foods, and also due to the increase of marketing advertises. The level of development is not led by one single factor, but by the combination of several. The key determinant factors for maturity in functional foods include: level of government support and compatibility of legislation with market growth, presence of a mature market for processed foods, level of consumer demand for supplementary nutrition, consumer confidence in products, health awareness, and threats to functional food (Justfood 2006; Research and Markets 2008; Euromonitor 2009). Functional foods compete in sales with organic, reduced fat, reduced salt, or reduced sugar foods. Indeed, controversy over the food chain, followed by numerous “food scares,” has increased the demand for “pure” organic foods, which could potentially damage functional foods sales, seen as “adulterated.” For functional food to be successful, it typically has to adhere to the following positioning (Figure 1): the health benefit has to appeal to a mass market and address general well-being issues; the health benefit has to be well communicated, either through understandable health claims, or through an active ingredient which is readily understood; the product must be competitive on all platforms, and not rely solely on its health benefits; it must also offer taste, convenience, and appropriate pricing. Although functionality allows for higher margins, it does not guarantee success by itself. Other aspects, such as brand name loyalty, advertising, promotion, quality control, competitors, and economic factors are also important. Regarding functional foods, it has been observed that modern consumers are increasingly interested in their personal health, expecting the food they eat to be healthy or capable of preventing illnesses. The popularity of dose-delivery systems for probiotic products has resulted in research efforts targeted to developing probiotic foods outside the dairy sector. New product categories, and thus novel and more difficult raw materials with regard to probiotics technology, are certainly the key research and development area for functional food markets. Current technological innovations include finding solutions for the stability and viability problems of probiotics in new food environments, such as fruits, cereals, and other vegetables (Farnworth and others 2007). Therefore, researches are important to develop new media for probiotic growth and development, increasing the number of products with functionality in the marketplace, and offering new options for all types of consumer’s demand and desire. Probiotics market Among the foods whose allegations of health have been widely promoted in the media during the last years, and that present multidimensional studies for technological and industrial uses, those with probiotic strains stand out (Lourens-Hattingh and Viljoen 2001). The definition of the term probiotic has evolved through Vol. 9, 2010—COMPREHENSIVE REVIEWS IN FOOD SCIENCE AND FOOD SAFETY 293 CRFSFS: Comprehensive Reviews in Food Science and Food Safety the years. The most recent definition says that probiotics are live microorganisms administered in amounts that positively affect the health of the host (FAO/WHO 2002; Sanders 2003). The global market for probiotic ingredients, supplements, and foods was worth $14.9 billion in 2007 and reached US$16 billion in 2008. Estimates target a total of US$19.6 billion on sales in 2013, a compound annual growth rate (CAGR) of 4.3%. Probiotics of the Lactobacillus genus accounted for the largest share, representing 61.9% of total sales in 2007 (Food Processing 2009). Food applications for probiotics are found mostly in dairy products, with yogurts, kefir, and cultured drinks representing the major categories. Yogurt products accounted for the largest share of sales, representing 36.6%, and scientific development of such products had shown the high sensory acceptance (Almeida and others 2008; Almeida and others 2009; Zoellner and others 2009); emerging food applications include probiotic cheese and ice creams (Cruz and others 2009a, 2009b), nutrition bars, breakfast cereal, infant formula, and many others. In accordance with a commercial research carried by Foodprocessing (2009), as a result of continued advertising and combined marketing schemes, mainly from processors of finished goods, the level of consumer awareness of different types of probiotics has improved significantly in the last 5 y. This has driven research efforts into the development of alternative delivery formats in the probiotics category that can appeal to a wider range of consumers. Foods and supplements manufacturers are also eager to join the bandwagon and apply probiotics in their existing products. According to a survey conducted with 2000 North-American consumers (Mintel Intl. Group 2009), 19% of adults in 2008 had purchased a pre/probiotic yogurt in the previous 3 mo, compared to 11% in 2006. Nearly twice as many women as men had consumed these products in 2008, at 24% and 13%, respectively. Individuals in the 45 to 54 age range were the largest purchasers, at 30%. According to Euromonitor (2008) data, the North-American probiotic spoonable yogurt market alone went from US$ 112 million in 2001 to US$ 294 million in 2006. Meanwhile, consumption of probiotics is equally strong in Europe. Euromonitor Intl. (2008) reports that between 2002 and 2007, consumption in Western Europe grew 13% CAGR, and consumption in Eastern Europe increased nearly 18% CAGR. Consumption in tones for 2007 in Western and Eastern Europe was 1125 and 10151, respectively; the numbers are forecasted to hit 1747 and 13205 by the year 2012 in those regions. European food and beverage probiotic market is expected to rise from its 2006 position of US$ 61.7 million to US$ 163.5 million by 2013. According to Euromonitor (2009), the probiotic yogurt market in Latin America grew 32% CAGR from 2005 to 2007, and accounted for 30% of total yogurt market value in 2007. It is very hard to find data that report sales based on nondairy probiotic products, once this category is relatively new in the marketplace. Moreover, they are not commonly found in many countries, such as in Brazil, where there is only one brand that markets one soy “yogurt” with different fruit pulps. It would be interesting if more data were available regarding worldwide sales of probiotic foods, so the industry could direct product development toward one specific segment of population or a certain type of well-acceptable product. products have just over 22% (LFI 2006). A total of 78% of current probiotic sales in the world today are delivered through yogurt. Fruit juices, desserts, and cereal-based products featuring probiotics may be other suitable media for delivering probiotics (Cargill 2009). Indeed, technological advances have made possible to alter some structural characteristics of fruit and vegetables matrices by modifying food components in a controlled way such as pH modification, fortification of culture media, among others (Betoret and others 2003). This could make them ideal substrates for probiotics culture, since they already contain beneficial nutrients, such as minerals, vitamins, dietary fibers, and antioxidants, while lacking the dairy allergens that might prevent consumption by certain segments of the population (Sheehan and others 2007). It is known that the allergy to dairy products affects negatively many people around the world. Traditions and economic reasons that limit the use of dairy products in developing countries, such as Japan, China, and some African countries, promote the idea of reducing milk components as vehicles for the probiotic agents or even replacing milk with other media, such as cereals, fruits, and vegetables. Lactose intolerance, cholesterol content, and allergenic milk proteins are the major drawbacks related to the intake of dairy products, which makes the development of new nondairy probiotic foods essential. Lactose intolerance: some considerations Lactose (4-O-β-D-galactopyranosyl-D-glucose) is a disaccharide sugar composed of glucose and galactose. It is unique to mammalian milks, which vary from almost undetectable concentrations in marine mammals to 7 g/100 mL in mature human milk. It is the 1st dietary sugar to which newborns are exposed. Lactose itself is a fermentable substrate, first being hydrolyzed by facultative or anaerobic microorganisms, allowing for anaerobic metabolism of the resultant simple sugars (Solomons 2002). The chemical structure of lactose is shown in Figure 2. Lactase is a hydrolase enzyme, produced in the small intestine, able to catalyze the hydrolysis of β-galactosides (such as lactose) into monosaccharides (glucose and galactose derived from lactose). Lactase is present in high quantities in the digestory tract of children, whereas in adults the quantity of such enzyme is decreased. The deficiency of one or more enzymes involved in lactose digestion may lead to metabolic disturbs known as lactose intolerance. Since there is no treatment that may increase the lactase producing ability, the symptoms must be controlled by the diet either by consuming milk substitutes or alternative products available on the market, so as to guarantee the maintenance of a good nutritional condition (Schaafsma 2008). Lactose intolerance consists of the absence of lactase production, which is responsible for hydrolyzing the lactose present in Nondairy probiotic products: why are they important? Nondairy probiotic products have a big worldwide importance due to the ongoing trend of vegetarianism and to a high prevalence of lactose intolerance in many populations around the world. However, there is no question that the dairy sector, which is strongly linked to probiotics, is the largest functional food market, accounting for nearly 33% of the broad market, while cereal Figure 2 --- Chemical structure of lactose. 294 COMPREHENSIVE REVIEWS IN FOOD SCIENCE AND FOOD SAFETY—Vol. 9, 2010 Functional foods . . . dairy products. Data on the incidence of lactose intolerance are not easily found. According to the Natl. Inst. of Kidney Disease and Diabetes (USA), affiliated to the American Inst. of Health, about 75% of the world population is lactose intolerant. This range is from less than 5% in Denmark, Britain, and Holland in northern Europe to > 90% in China, Korea, Thailand, and among the Yoruba of Nigeria and Native Americans of North America (Solomons 2002). However, probably this estimate is, to a large extent, an approximation, since diagnostic methods vary and also the number of people examined tends to be small and frequently includes hospitalized patients. In accordance with Alm (2002), in North Europe the number of lactose-intolerant individuals is around 5%, in some African countries it reaches 90%, while in the Unites States of America it is around 30% of the adult population. In Brazil, although there are few studies, the incidence of lactose intolerance is between 46% and 67%; recently, a research reported that the yogurts available in Brazilian market are unsuitable for consumption by lactose intolerant individuals, due to the small reduction of their lactose content during the commercial shelf-life time (Batista and others 2008). However, it is known that probiotic bacteria are not able to supply lactase in enough amounts, but the yogurt starter cultures themselves might provide enough quantity of lactase for the consumers, and hence yogurts and cheeses may be consumed by lactose-intolerant individuals (Ouwehand and others 2003). Indeed, the cultures in these products can alleviate lactose intolerance on the residual lactose but the effectiveness of this beneficial effect may vary as a function of the quantity of cells in the product, the amount of lactase produced, the level of lactase that remains active after passage through the stomach, and the release level of lactase in the gastrointestinal tract (Sanders 1993). This considerable variation in lactose intolerance is mainly due to ethnic differences. Some other European and Asiatic countries present a high percentage of lactose-intolerant individuals, as shown in Table 1. Hence, it is evident that the development of lactose-free products is a necessary task; moreover, dairy-free ingredients are very suitable for markets with a high prevalence of lactose-intolerance. In accordance with Pelto (2000), there are lactose intolerant and milk-sensitive individuals. When dietary lactose is not hydrolyzed into its component simple sugars in the small intestine, so that the latter can be absorbed across the intestine and used for fuel in the body, a situation of lactose maldigestion is produced. The lactose passes out of the small bowel in its intact, undigested form and enters the large intestine. There it serves as a fermentable substrate for the colonic microflora. Lactose and its split products serve as osmotically active molecules, drawing secretion of water into the intestinal lumen to balance the osmolarity pressures. This accumulation of water produces dehydration and electrolyte imbalance on the systemic side and watery stools on the intraintestinal side. The fermentation of the sugar adds a gaseous component to the process; evolution of carbon dioxide, hydrogen, and methane produce the bloating, cramping, and flatulence (Stephens and others 1983). This may lead to some inconvenient side effects, such as allergic reactions, bellyache, and flatulence, contributing to a low quality of life. The intensity of such effects is dependent on the quantity of lactose ingested. In general, lactose-intolerants show inadequate ingestion of calcium and other milk-provided nutrients, since they consume limited amounts of dairy products, which increase the probability of developing osteoporosis. Therefore, nondairy probiotic products should provide, to some extend, a minimum content of calcium. How can nondairy probiotic products be developed? Innovation is today’s business mantra. Pundits proclaim daily that the only hope for business survival is the ability to continue innovating. In this context, the development of new nondairy probiotic food products turns out to be increasingly challenging, as it has to fulfill the consumer’s expectancy for products that are simultaneously relish and healthy (Shah 2007). According to Jousse (2008), new product development is a constant challenge for both scientific and applied research, and it has been observed that food design is essentially a problem of optimization to generate the best formulation. For this purpose, industries need to determine the basic formulation for each product, but this task is not easy, especially when many factors are associated to multiple features that need to be achieved. Second, the determination of optimum levels of key ingredients is necessary to obtain suitable sensory and physicochemical characteristics, extended shelf life, chemical stability, and reasonable price. Developing a new dairy-free probiotic food is an expensive process. Food companies have traditionally funded research for new food product formulations, but the stakes are higher Table 1 --- Prevalence of lactase deficiency, in percentage, for lactose-free products, for both food companies and consumers (Walzem 2004). Product development requires detailed knowlof the worldwide adult population. edge of the products and the customers, which is why quantitative and qualitative marketing studies must be carried out % of the adult population Country afflicted by lactose intolerance before launching any product on the market (Beardsworth and Keil 1992). The high reported failure rates for new international France 30 to 40 functional foods suggest a failure to manage the customer knowlGermany 15 to 20 edge effectively, as well as a lack of knowledge management Russia 20 to 30 between the functional disciplines involved in the new product Finland 15 to 20 development process (Jousse 2008). The methodologies that adSweden <5 vance a firm’s understanding of customer’s choice motives and Greece 70 to 80 values, and its knowledge of management process, can increase Ethiopia 80 to 90 the chances of new product success in the international marNigeria 80 to 90 ket. The commercial success of dairy-free probiotic products ulChina 90 to 100 timately depends on taste, appearance, price, and health claim Japan 95 to 100 appeal to consumers. They need to receive a comprehensible Índia 60 to 65 and reasonable message about the physiological effects of probiIsrael 70 to 80 otics in humans, without appearing to be exaggerated; moreover, USA (white) 10 to 15 all the factors mentioned previously influence directly the conUSA (black) 65 to 70 sumers’ attitudes toward effective purchase, which is necessary Mexico 50 to 60 for the maintenance of industry. For these reasons, in summary, Uruguay 60 to 65 the food industry takes into consideration many variables to develop or reengineer nondairy probiotic products, such as sensory Source: Modified from Alm (2002). Vol. 9, 2010—COMPREHENSIVE REVIEWS IN FOOD SCIENCE AND FOOD SAFETY 295 CRFSFS: Comprehensive Reviews in Food Science and Food Safety Non-dairy probiotic products development Assembling the ideas Prototype making Microorganism screening Health benefits studies (in vivo, in vitro) Ability to grow in a non-dairy matrix Generally Regarded as Safe Non-pathogenic Formulation development Functional claim Ingredient selection Development process Preservation methods Packaging Design and functionality Shelf-life and stability Sensory and market studies Quantitative Qualitative Obtaining a health claim In vitro assays Clinical studies Dose effects Safety issues Figure 3 --- Basic steps to be considered by nondairy probiotic food producers for product development. acceptance, stability, price, chemical, and functional properties, as illustrated in Figure 3. It is noteworthy that governments are currently tolerating the simple statement that the products contain probiotic bacteria. Health agencies worldwide may eventually demand other assays to a firm displays on the label that a product presents the probiotic effects. Some developed lactose-free probiotic products The consumption of beverages and foods that contain probiotic microorganisms is a growing worldwide trend (Verbeke 2005). Even though fermented dairy products are generally good matrices for the delivery of probiotics to humans, other foods have been examined for their potential as probiotic carriers. Mayonnaise, soymilk, meats, baby foods, ice creams, fruit drinks, vegetable drinks, and many others have already been proposed (Champagne and others 2005; Homayouni and others 2008). 296 There is a wide variety of traditional nondairy foods developed around the world. Many of them are nonalcoholic beverages manufactured with cereals as main raw materials. Boza (made from fermented cereals) is a cold beverage consumed in Bulgaria, Albania, Turkey, and Romania. Bushera is the most common traditional cereal-based beverage prepared in the Western highlands of Uganda. Mahewu (amahewu) is a sour beverage made from corn meal, found in Africa and some Persian Gulf countries. Pozol is a refreshing beverage, widely produced in the Southeastern México, made with cocoa and cornmeal. Togwa is a starch-saccharified traditional beverage consumed in Africa that has been used as a probiotic medium (Prado and others 2008a). Other nondairy products available in the marketplace are effervescent tablets, chewable tablets, and drinking straws. Farnworth (2004) pointed out the potential of root crops, legumes, shrimp, cassava, different types of vegetable flours, fish, fruit seeds, meats, fungi-based substrates, as well as milk from a variety of animals for the development of new probiotic foods. These foods can be used as templates for innovation, where traditional starter cultures can be replaced by probiotic ones. Bifidobacterium species and lactic acid bacteria, especially Lactobacillus strains, are widely used in food production, not only in fermentation of vegetables, sausages, and milk, but also in fruit-based and vegetable-based products, such as carrot, beet, and celery (Karovicova and others 2002), garlic (Castro and others 1998), green olives (Sanchez and others 2000), green cucumber juice (Lu and others 2001), onions and peas (Karovicova and others 1993), alfafa, clover, and galega (Shurkhna and others 2006), and cereals (Angelov and others 2006). Most part of the mentioned studies was carried in Japan or in Europe, and almost none considers the sensory acceptability of such products by potential consumers. Other nondairy products include acidophilus soybased drink, frozen desserts, vegetable-based drinks, puddings, among others, as shown in Table 2. Despite potential sensory challenges, there is a genuine interest in the development of fruit-juice based functional beverages fortified with probiotic ingredients. Fruit juices have been suggested as ideal media for probiotic growth because they inherently contain essential nutrients, they are good-looking and have good taste (Luckow and Delahunty 2004; Champagne and others 2005; Sheehan and others 2007). Fruits and vegetables are rich in minerals, vitamins, dietary fibers, antioxidants, and do not contain any dairy allergens that might prevent usage by certain segments of the population. Application of probiotic cultures in nondairy products represents a great challenge. Probiotic viability in the food matrix depends on factors, such as pH, storage temperature, oxygen levels, and presence of competing microorganisms and inhibitors. It is important that the formulation maintains the activity and viability of the probiotic for extended periods of time (Shah 2007). Since the probiotic cultures are included as ingredients to these kinds of products, they do not usually multiply, which sets great demands for the probiotic stability. Factors like water activity, oxygen tension, and temperature become increasingly important when dealing with these kinds of products. Storage at room temperature, which is common for many types of nondairy products, such as cereal products, drinks, confectionary, and so on, can create an overwhelming challenge for probiotic stability (MatillaSandholm and others 2002). Adding probiotics to fruit-based and cereal-based matrices is more complex than formulating dairy products, because the bacteria need protection from the acidic conditions in these media. Microencapsulation technologies have been developed and successfully applied using various matrices to protect the bacterial cells from the damage caused by the external environment. It is the process by which small particles or droplets are surrounded COMPREHENSIVE REVIEWS IN FOOD SCIENCE AND FOOD SAFETY—Vol. 9, 2010 Functional foods . . . Table 2 --- Some nondairy probiotic products recently developed. Category Product Reference Fruit and vegetable based Vegetable-based drinks Fermented banana pulp Fermented banana Beets-based drink Tomato-based drink Many dried fruits Green coconut water Peanut milk Cranberry, pineapple, and orange juices Ginger juice Grape and passion fruit juices Cabbage juice Carrot juice Noni juice Onion Probiotic banana puree Nonfermented fruit juice beverages Blackcurrant juice Lambo and others (2005), Rakin and others (2007) Tsen and others (2004) Tsen and others (2009) Yoon and others (2005) Yoon and others (2004) Betoret and others (2003) Prado and others (2008a) Mustafa and others (2009) Sheehan and others (2007) Chen and others (2008) Saarela and others (2006) Yoon and others (2006) Nazzaro and others (2008) Wang and others (2009) Roberts and Kidd (2005) Tsen and others (2009) Renuka and others (2009) Luckow and Delahunty (2004) Soy based Nonfermented soy-based frozen desserts Fermented soymilk drink Soy-based stirred yogurt-like drinks Heenan and others 2005 Donkor and others (2007) Saris and others (2003) Cereal based Cereal-based puddings Rice-based yogurt Oat-based drink Oat-based products Yosa (oat-bran pudding) Mahewu (fermented maize beverage) Maize-based beverage Wheat, rye, millet, maize, and other cereals fermented probiotic beverages Malt-based drink Boza (fermented cereals) Maize, sorghum, and millet malt fermented probiotic beverages Millet or sorghum flour fermented probiotic beverage Helland and others (2005) Boonyaratanakornkit and Wongkhalaung (2000) Angelov and others (2006) Martensson and others (2002) Blandino and others (2003) McMaste and others (2005) Wacher and others (2000) Blandino and others (2003) Other nondairy foods Starch-saccharified probiotic drink Probiotic cassava-flour product Meat products Dosa (rice and Bengal gram) by a coating to produce capsules in the micrometer to millimeter range known as microcapsules, which allows the probiotic bacteria to be separated from its environment by a protective coating and, therefore, this protection increases the viability of such bacterial strains (Ding and Shah 2009a, 2009b). More research needs to be carried out to find suitable ingredients for microencapsulation and hence probiotic viability in nondairy matrices. Soy-based probiotic products: consumer’s attitude, market, and science development The demand for alternatives to dairy products is growing due to problems with intolerance and allergy, desire for vegetarian alternatives, and so on, and hence the interest in soy-based foods has developed. It should be stated that there are numerous nondairy allergies linked to soy, gluten, and vegetables, which means that milk-based products are not the only ones that may confer allernenicity on consumers. Probiotic yogurts are now being marketed, and consequently it would be desirable to know if probiotic bacteria can also be incorporated into soy-based yogurt-type fermentations (Farnworth and others 2007). Kedia and others (2007) Moncheva and others (2003) Blandino and others (2003) Muianja and others (2003) Oi and KIitabatake (2003) Molin (2001) Kröckel (2006) Soni and others (1986) Probiotic products developed with soy extract mixed with fruit juices are the new generation of foods on the market, which is a convenient way to include soy protein in the basic diet (Champagne and Gardner 2008). From 1992 to 2008, soy foods sales worldwide have increased from US$ 300 million to almost US$ 4 billion. This increase can be attributed to new soy food categories being introduced, soy foods being repositioned in the marketplace, new customers selecting soy for health, and philosophical reasons (Soyfoods 2009). In the United States, marketing of beverages formulated with soy, has doubled since year 2000, becoming an important category in the market, and accumulating sales higher than US$ 100 million annually (Beverage Marketing Corp. of New York 2005). According to Euromonitor (2009), soy yogurt represents 12% of the US$ 3.7 billion of the global market for soy-based dairy alternatives in 2008 with a growth of 17% annually. Europe has seen a double digit growth in annual sales of soy-based dairy alternatives in the past couple of years. In accordance with Euromonitor (2008), the market of probiotic soy “yogurts” represented 12% of the total sales of soy-based products in 2005, with an increase of 17% annually. As a suitable alternative for probiotic dairy Vol. 9, 2010—COMPREHENSIVE REVIEWS IN FOOD SCIENCE AND FOOD SAFETY 297 CRFSFS: Comprehensive Reviews in Food Science and Food Safety products, soy-based foods that contain probiotic strains have been consumed. In accordance with a research carried out by the United Soy Board (2009), 32% of North Americans consume soy foods or soy beverages at least once a month, on par with 2006 through 2008; approximately 33% of U.S. consumers seek out products containing soy and approximately 31% of consumers are aware of specific health benefits of soy in their diet; on an aided basis, consumers are most aware of the health benefits of soy in relation to weight management (31%), reduced risk of heart disease (27%) and some cancers (20%); over 34% of consumers said they are aware of the FDA claim that consuming 25 g of soy protein per day reduces the risk of coronary heart disease; and 84% of consumers perceive soy products as healthy. Recently a study conducted by Wagar and others (2009) reported the immunomodulatory properties of fermented soy prepared with lactic acid bacteria by a modulation of intestinal epithelial cells Interleukin-8 (IEC IL-8) production in vitro, suggesting the importance of soy probiotic products for consumer’s health. Picking up on the trend in dairy products, new lactose-free probiotic-containing products have been launched, particularly in fruit-based drinks and cereals. Soy is an excellent candidate for such products. A 1st benefit of soy beverage fermentation is the reduction of its “beany” flavor and chalkiness. Soy is also considered a good substrate for functional foods, since fermentation by probiotics has the potential to (1) reduce the levels of some carbohydrates possibly responsible for gas production in the intestinal system, (2) increase free isoflavone levels and (3) favor desirable changes in bacterial populations in the gastrointestinal tract. Soy also benefits bone health (Champagne and others 2009). Moreover, Larkin and others (2007) showed that a combination of soy with either a probiotic or a prebiotic resulted in significant lipid lowering effect for both total and low-density lipoprotein (LDL). This effect is not related to isoflavone bioavailability, since the bioavailability of daidzein and genistein was not affected by probiotic or prebiotic consumption and were not associated with lipid changes. Until the 1st half of the 1990s, products containing watersoluble soy extract, such as juices and ices creams, were not well accepted due to the astringent flavor. However, since that time, international industries have made use of new technologies, as well as genetic changes and use of successful ingredients, in the attainment of products with improved sensory qualities (Behrens and others 2001). Throughout this decade, new palatable soybased nondairy probiotic products have been developed by food industries and a huge demand is observed due to the spreading of the health benefits attributed to their consumption (Helland and others 2005; Donkor and others 2007). Soy and its derivatives have received attention from researchers worldwide, mainly due to the amount and quality of its protein. Soy protein presents a good amino acid profile; however, cysteine, cystin, and methionine are limiting. Moreover, soy is a source of soluble fiber, magnesium, phosphorus, vitamins K, riboflavin, thiamine, and folic acid. Soy contains isoflavones and other flavonoids, compounds with strong antioxidant activity, capable of acting in the prevention of nontransmissible chronicdegenerative diseases (Wang and others 2006), such as many types of cancer. Studies have disclosed that phenolic compounds, generally free aglycones and some isoflavones found in soy-based fermented foods, such as missô, natô, and tempê, possess higher antioxidant activity than those that were not fermented, evidencing the importance of the development of soy products submitted to fermentative processes (Esaki and others 1994). Soybean contains oligosaccharides—raffinose and stachyose —that are not digested by humans and, therefore, can cause flatulence. However, these α-galactosides are sources of carbon for 298 the growth of various Lactobacillus species, such as Lactobacillus acidophilus and Lactobacillus delbruecki subsp. bulgaricus, as well as Bifidobacterium species (Scalabrini and others 1998). Therefore, soy products can be a good culture medium for inoculation and growth of probiotic strains (Wang and others 2003). Soymilk itself has been reported to support the growth of bifidobacteria, but at slower rates than those in reconstituted skim milk. Bifidobacteria have α-galactosidase activity, which enables them to utilize sugars such as raffinose and stachyose, and sufficient proteolytic activity to support growth in soymilk (Farnworth and others 2007). According to Champagne and others (2009), the development of a fermented soy product containing probiotics requires strain selection for the ability to grow in the substrate, as well as the ability to compete or even establish a synergy between strains. The main probiotic bacteria studied for growth in soy beverages are Lactobacillus acidophilus, L. fermentum, and bifidobacteria. Otherwise, L. rhamnosus was shown to grow slowly in milk, but a discrepancy occurs in soy, and its growth was better in a commercial soy beverage than in milk. The same researcher reported that L. lactis R0187 is a strain with relatively good growth rates on soy carbohydrates, but its growth in commercial soy beverage is slower than other lactobacilli. There is every reason to believe that soy beverages and yogurts will be the next food category for which the healthy bacteria will make their mark. Likely candidates are chilled fruit juices or fermented vegetable juices. The probiotic microorganisms also have been directly incorporated into beverages. The key to the development of this 2nd generation of the probiotic products is a special direct liquid inoculation system. It allows food producers to add the probiotic bacteria directly to the finished food product, which can lead to a higher number of viable microorganisms, and thus increase its functionality (Prado and others 2008a). Scientific research has shown that yogurts and water-soluble soy-containing-fermented beverages present a good sensory acceptance by potential consumers: soy fermented yogurts garnered high scores of appearance, texture, and flavor, with sensory acceptance of 82.5% (Marinho and others 1994); an iron-fortified soy yogurt presented suitable hedonic scores for creaminess and flavor (Umbelino and others 2001); water-soluble soy extract fermented beverages with bifidobacteria showed superior acceptability compared to that fermented with L. casei (Shimakama and others 2003); a soy yogurt product supplemented with oligofructose and inulin presented acceptance index above 70% (Hauly and others 2005). Therefore, researches have shown that probiotic soy-based products in combination with fruit juices are successful in the maintenance of both probiotic and sensory properties. A higher demand of these products indicates that consumers have incorporated them into their regular diet, changing their attitude toward soy and its by-products, and also changing their expectations with regard to new probiotic soy-based products available in the marketplace. Juice probiotic products: consumer’s attitude, market, and science development Consumer convenience and health represent the 2 most important trends in the food industry. During the past 2 decades, probiotic health-promoting microorganisms have been increasingly included into commercial dairy products in a response to the consumer demand for healthy food options that improve overall health (Menrad 2003). Due also to this reason, several worldwide food companies have begun researching possible probiotic enhanced line extensions. Recently, the beverage market is moving a little bit more away from its carbonated drinks, which are well known to exert no too many positive effects on the human COMPREHENSIVE REVIEWS IN FOOD SCIENCE AND FOOD SAFETY—Vol. 9, 2010 Functional foods . . . wellness. In Europe and Japan, probiotic dairy products dominate the relative market, but in the world the biggest food companies are trying to open new windows of opportunity for probiotic R segment. In the United States, Kraft launched in 2008 the 1st mass-distributed shelf stable probiotic nutrition bar, focusing its production mainly by using the bacteria L. plantarum 299v. In R Sweden, the Skane company launched an extension of “ProR Viva ” probiotic fruit juice drink, based on clinical evidence that such microorganism can improve iron intake in women. The product differs little from the parent brand, containing a little bit higher amount of iron (Nutraceuticals World 2008). Some technical challenges have suggested that fruit juice could serve as a good medium for functional ingredients like probiotics (Nazzaro and others 2008). Fruit juice can be certainly positioned as a healthy food product, due to its great amount of healthy components like vitamins, antioxidants, and polyphenols that exerts several positive benefits on the human health. It has also been suggested as a novel, appropriate medium for fortification with probiotic cultures already being positioned as a healthy food product, and frequently consumed and loyally by a large percentage of the global consumer’s population (Tuorila and Cardello 2002). The sensory evaluation of the presence of probiotics in fruit juice systems and has vital commercial importance. It is necessary to understand the sensory impact that probiotic cultures have on nondairy systems, and to determine how probiotic fortification influences the consumer acceptance and preference for fruit juice, in terms of appearance, aroma, texture or taste, with the aim to convey the direction to an optimal development and formulation of these products. Generally, there is a remarkable flavor and aromatic impact associated with functional ingredients, such as the presence of acidic phenols, flavonoids, terpenes, isoflavones, tannins, which, on the whole, can characterize the resulting functional product in terms of “bitterness” or “astringency” (Drenowski and others 2002). The sensory impact of probiotic cultures has not yet been deeply studied; however, it can be assumed that products fortified with these functional ingredients would have different taste profiles compared to the conventional, nonfunctional products. Study performed by Luckow and Delahunty (2004) showed that consumers have been able to distinguish a sensory difference between functional orange juice containing probiotics and their “conventional” counterparts. Consumers described functional orange juice as containing “dairy,” “dirty,” and “medicinal” flavors if compared to conventional juice, that was preferred to the functional one. Due to their negative perceptions of the sensory characteristics of functional juices, consumers indicated that they would not be willing to consume the juice in the quantity or frequency required to obtain the health benefits associated with functional ingredients. However, the study did not give to the consumers all the necessary information about the health benefits associated with the functional juice products, neither the interaction between product information and product liking could be measured. Sometimes, in fact, consumers are influenced to associate “healthy” foods with unacceptable flavors, assuming in their mind that sensory pleasure must be sacrificed to achieve a healthy diet (Tuorila and Cardello 2002). Then, it is possible that consumers would immediately judge products labeled as “probiotic” as less attractive than nonprobiotic juices. However, other studies showed that taste is the primary driver for food selection, followed by health considerations (Tepper and Trail 1998; Tuorila and Cardello 2002), suggesting that consumers would judge the acceptability of a product based on taste, rather than predetermine and preconception acceptability based on the health claims, and visible product information. Perhaps consumers would evaluate fruit juice products in a unique manner altogether. Since juice is already perceived as healthy, it is unclear whether consumers would have negative biases about the flavor and acceptability of a fortified juice, or whether functional juices would be perceived as more favorable to the consumer. Despite potential sensory modifications, there is an authentic interest to the development of fruit-juice-based functional beverages, fortified with probiotic microorganisms. Indeed, in the last years many companies have released more products with “good-for-you” ingredients, such as antioxidant rich-fruit juices and probiotics well known recognized for their digestive and immune health benefits. These functional beverages, being dairy free, soy free, wheat free, and vegan, meet a considerable preference by a large segment of the population. It is of important commercial interest to compensate for the off-flavors present in fermented fruit juices, and to improve the sensory acceptability, driving the consumer to the consumption of the product. Obviously, product information is an important part of marketing and consumer education, and has been shown to impact the scaling behavior of consumers (Levis and Chambers 1996; Di Monaco and others 2003; Stein and others 2003). Specific information concerning the addition of probiotic cultures to the juices, and their subsequent health benefits of the probiotic ingredients had a significant effect on consumer liking. Different attempts can be made to formulate a probiotic fruit juice that could meet the favor of the consumers and to better stabilize the microorganisms in a nondairy product, where generally they are less stable and are more sensitive to different adverse environments (Chou and Weimer 1999). Masking is one technique that has been used to reduce the sensations of unpleasant odors and flavors in foods and it has been performed successfully through the addition of new substances or flavors to juices (Reineccius 2000), and is therefore supposed to be capable of reducing the negative sensory attributes contributed by probiotic cultures. The addition of tropical fruit juices, mainly pineapple, but also mango or passion fruit, might positively contribute to the aroma and flavor of the final product and might avoid the identification of probiotic off-flavors by consumers (Luckow and others 2006). The influence of exposure has been identified in many consumer studies (Bertino and others 1986; Stein and others 2003), whereby preference ratings have been shown to be enhanced or reinforced with exposure. Furthermore, when the frequency of exposure to a food stimulus is increased, food stimuli have been shown to be better liked (Pliner 1982). Therefore, repeated exposure and increased familiarity to sensory off-flavors, may influence consumer attitudes in a positive way, therefore increasing willingness to consume probiotic juices. Nonsensory techniques have proven useful in enhancing the sensory quality of products despite off-flavors. Providing consumers with information about the health benefits associated with probiotic cultures may also improve the perceived sensory quality of probiotic juices. Health information has been shown to be a vital tool in the consumer acceptance of a variety of food products (Kahkonen and others 1995; Tuorila and others 1998; Deliza and Silva 2003). After being provided with information about the health benefits of probiotic cultures, the uncharacteristic aromas and flavors might play a positive role in functional foods, as markers for the probiotic ingredients, and as proof of the action of the products (Juttlestad 1998). Finally, a method of producing probiotic fruit juice is by using, during the fermentative steps, probiotics previously immobilized in different coating materials. Even if, as previously described, the resulting taste and aroma of the product could result in terms of a too strong “bitterness,” acidity, and astringency, the addition of other fruit juices can give rise to a product that can meet the approval of the consumers. This can be seen also by consumer as a further way to protect Vol. 9, 2010—COMPREHENSIVE REVIEWS IN FOOD SCIENCE AND FOOD SAFETY 299 CRFSFS: Comprehensive Reviews in Food Science and Food Safety and preserve the probiotic cultures by all the stress that they can encounter during the fermentation and during the subsequent storage at 4 ◦ C (Champagne and others 1994; Favaro-Trindale and Grosso 2002; Homayouni and others 2007). Chandramouli and others (2004) and Giulio and others (2005) found that encapsulation of LAB helped overcome inactivation during drying or exposure to artificial gastric conditions. Tsen and others (2004) used immobilized L. acidophilus to ferment banana puree and observed that the number of viable cells during fermentation was increased significantly relative to free cells. Recently, Nazzaro and others (2009) immobilized L. acidophilus in an alginate–prebiotic mixture and incubated it in carrot juice. Encapsulation protected L. acidophilus from exposure to simulated gastric conditions; minor alterations in viability and the protein profile occurred after incubation in pancreatic juice. For free cells, viability decreased significantly and the expression of numerous proteins was lost after incubation in gastric and pancreatic juice. Thus, encapsulation preserved probiotic bacterial viability and activity; the addition of prebiotic components could enhance the functional properties of food products containing this formulation. Indeed, data by Corcoran and others (2005) showed that lactobacilli bacterial cells survive much better an acid environment if they have a carbohydrate such as fructans that can be assimilated and metabolized. Perspectives The future viability and success of functional foods in the marketplace depend on several elements. The key issue is consumer acceptance of such products. For consumers to agree to pay the cost associated with functional foods, they must be convinced by its health claims through clear, truthful, and unambiguous messages. Probiotics represent one of the largest functional food markets. Most of the available products are some form of dairy, such as milk, ice cream, yogurt, cheese, and frozen desserts, despite the continuously growth of the nondairy sector, with products like soy-based drinks, fruit-based foods, and other cereal-based products. Among the nondairy probiotic products, those made with soy stand out because of the inherently health benefits of soy, linked to the presence of isoflavones, and the beneficial changes in bacterial populations in the gastrointestinal tract, caused by the presence of probiotic microorganisms. Sales and marketing of probiotic soy products, such as yogurts-like, blends with fruit juices and fermented beverages, have increased during the past decade, showing a trend to the development of new products with suitable sensory and nutritional appeal, and beneficial properties, when regularly consumed. 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