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Propaganda
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
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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.
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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).
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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
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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
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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
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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. Both nondairy (in general) and
soy-based probiotic products represent a huge growth potential
for the food industry, and may be widely explored through the
development of new ingredients, processes, and products.
For this purpose, new studies must be carried out to: test ingredients, explore more options of media that have not yet been industrially utilized, reengineer products and processes, and show
that lactose-intolerant and vegetarian consumers demand new
nourishing and palatable probiotic products.
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