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CHAPTER THREE

Dairy foods and positive impact


on the consumer’s health
Silvani Verrucka, Celso Fasura Balthazarb, Ramon Silva Rochab,c,
Ramon Silvab,c, Erick Almeida Esmerinob, Tatiana Colombo Pimenteld,
Mo^ nica Queiroz Freitasb, Marcia Cristina Silvac,
Adriano Gomes da Cruzc,*, Elane Schwinden Prudencioa
a
Universidade Federal de Santa Catarina (UFSC), Departamento de Ci^encia e Tecnologia de Alimentos,
Florianópolis, Brazil
b
Universidade Federal Fluminense (UFF), Faculdade de Veterinária, Niterói, Brazil
c
Instituto Federal de Educação, Ci^encia e Tecnologia do Rio de Janeiro (IFRJ), Departamento de Alimentos,
Rio de Janeiro, Brazil
d
Instituto Federal do Paraná (IFPR), Campus Paranavaı́, Paranavaı́, Brazil
*Corresponding author: e-mail address: food@globo.com

Contents
1. Introduction 96
2. Fermented milks 98
2.1 Yogurt 98
2.2 Kefir 105
3. Cheese 112
3.1 Nutritional value of cheese 113
4. Butter 121
4.1 Beneficial health compounds in butter 123
4.2 Nutritionally modified butter 129
5. Ice cream 132
6. Dairy desserts 141
7. Conclusions 145
References 145
Further reading 164

Abstract
The objective of the present chapter was to demonstrate the state of the art in the
recent advances in nutritional and functional components of dairy products research.
In this chapter, the main mechanisms responsible and essential for a better understand-
ing of nutritional and functional values of the components of milk and dairy products
are highlighted. It also includes a discussion about the positive impacts of fermented
milk, cheese, butter, ice cream, and dairy desserts components on the consumer’s
health.

Advances in Food and Nutrition Research, Volume 89 # 2019 Elsevier Inc. 95


ISSN 1043-4526 All rights reserved.
https://doi.org/10.1016/bs.afnr.2019.03.002
96 Silvani Verruck et al.

1. Introduction
Dairy products had been an important part of the human diet since
animal domestication about 13,000 years ago (Balthazar, Pimentel,
Ferrão, et al., 2017) and are part of the official nutritional recommendations
in many countries worldwide (Rozenberg et al., 2016). Dairy products have
long been advertised as being excellent sources of nutritional components
and as a part of a well-balanced diet. Many investigations have suggested
benefits from dairy products beyond the classic “building strong bones.”
These advantageous effects arise from the proteins, minerals, vitamins, lipids,
and carbohydrates in dairy products (Tunick & Van Hekken, 2015). For
example, World Health Organization/ Food and Agriculture Organization
of the United Nations (WHO/FAO) established the recommended nutrient
intake (RNI) of 1000 mg/d of calcium for adults (Rippin, Hutchinson,
Jewell, Breda, & Cade, 2017). Numerous national nutritional recommenda-
tions suggest the consumption of three servings of dairy products per day,
such as a glass of milk, a portion of cheese and yogurt, resulting in an amount
that provides the recommended daily intake of calcium (Rozenberg
et al., 2016).
Dairy products represent good dietary sources of calcium due to their
high absorptive rate, availability and relatively low cost, which makes the
regular consumption of dairy products feasible. They provide more calcium,
protein, magnesium, potassium, zinc, and phosphorus per calorie than any
other typical food found in the adult diet (Rizzoli, Abraham, & Brandi,
2014). Under normal dietary conditions, about 30–40% of the calcium
contained in milk and cheese are absorbed in the gut either through
vitamin D-dependent transport across the duodenum, facilitated diffusion
or under the influence of lactose in the distal small intestine via the paracellular
route. Also, the casein phosphopeptides (CPP) and lactose in dairy foods can
facilitate intestinal calcium absorption (Wongdee & Charoenphandhu, 2015).
The digestibility values of milk protein are about 95%, whereas
casein alone is about 94.1%, being higher than those of soy, pea, wheat,
lupin, and rapeseed proteins (91.5%). Milk protein is also important for
building and maintaining muscle mass, notably the amino acids in whey
protein (Rutherfurd, Fanning, Miller, & Moughan, 2015). The caseins
facilitate the absorption of calcium and phosphate in the small intestine
and are the main substrates for production of bioactive peptides, such as
angiotensin-converting enzyme (ACE), thus, dairy products were found
Dairy foods and positive impact on the consumer’s health 97

to be cardioprotective; and minor milk protein lactoferrin has anticancer


properties (Barrubes et al., 2018).
Milk ingestion causes in some people, symptoms of bloating, abdominal
pain, flatulence, and diarrhea that can be severe enough to prompt avoid-
ance of all dairy foods. The symptoms are caused by a deficiency of the
enzyme lactase, responsible to break down lactose into galactose and
glucose for intestinal absorption, because undigested lactose increases the
osmolarity in the small intestine and enters the colon where it is fermented
by the resident microbiota, resulting in gastrointestinal symptoms
(Szilagyi & Ishayek, 2018). Fermented milks, such as yogurts, and hard
cheeses contain more predigested lactose and may be more readily tolerated
than fluid milk. The bacterial lactase survives the acidic conditions of the
stomach, apparently being physically protected within the bacterial cells
and by the buffering capacity of the yogurt. The slow gastrointestinal transit
time allow the bacterial lactase to be active, digesting lactose from yogurt,
which is enough to prevent symptoms in lactose intolerant people
(Savaiano, 2014).
A tremendous amount of research about dairy products has been done on
traditional and novel ingredients, starter cultures and probiotics, prebiotics
and symbiotic, and their effects on consumers health. Ingestion of probiotic
microorganism through dairy products can result in both prophylactic and
therapeutic effects. Probiotic benefits have mainly been related to the health
of the gastrointestinal tract and by exclusion of pathogens through compe-
tition for nutrients and binding sites and by the in-situ production of
antimicrobials (Hill et al., 2014). As for the probiotics, several studies on
prebiotics and symbiotics have reported that these components are clinically
effective in maintaining the balance of gastrointestinal microbiota and
improving health conditions. Prebiotics are fermentable fibers, such as inulin
and oligofructose, which selectively feed beneficial bacteria in the intestinal
microbiota, maintaining a healthy microbiome environment. Probiotics are
supplements with live microbes, showing immune supportive effects in the
gastrointestinal tract. However, both pre- and probiotics have been reported
to work best in combination. This combined effect results in a symbiotic
product. Prebiotic components remain unaltered in the gastrointestinal
tract, reach the large intestine intact and are selectively fermented to give
beneficial effects (Mohanty, Missra, Mohapatra, & Sahu, 2018).
Novelties about the nutritional values and functional components of
other dairy products, such as, cheese, butter, ice cream and dairy desserts,
have been highlighted and discussed in the present chapter.
98 Silvani Verruck et al.

2. Fermented milks
Fermented milks are products obtained by fermentation of milk using
starter cultures. Several products fall into this category, such as yogurt,
acidophilus milk, fermented or cultured milk, kumys, kefir, fermented curd,
buttermilk, sour cream, among others (Pimentel, Antunes, et al., 2017).

2.1 Yogurt
Yogurt leads the category of fermented milks in terms of volume of
production and research activity, with innovations in ingredients, starter,
and probiotic cultures, types of packaging, sensory properties, composition,
manufacturing methods, addition of flavorings, among others (Aryana &
Olson, 2017).
Yogurt is the product resulting from the fermentation of milk by proto-
symbiotic cultures of Lactobacillus bulgaricus and Streptococcus thermophilus.
However, in some countries, the term yogurt is restricted to products made
exclusively by the two cultures, while other countries also allow adjunct
probiotic cultures to be labeled as yogurt. Therefore, other lactic acid
bacteria can also be added to contribute to the characteristics of the final
product (Chandan, Gandhi, & Shah, 2017), such as L. acidophilus, L. casei,
and Bifidobacterium spp. (Pimentel, Antunes, et al., 2017). Yogurt is a dairy
product much consumed because of its high nutritional value, pleasant taste,
characteristic texture and perceived safety (Chandan et al., 2017). The
fermentative process increases the nutritional value, resulting in products
with higher levels of vitamin B, conjugated linoleic acid (CLA) (Balthazar
et al., 2016) and bioactive peptides than milk and other unfermented dairy
products (Donovan & Hutkins, 2018).
The beneficial health effects associated to yogurt consumption are related
to the presence of viable bacteria and their metabolites and its composition
(protein, calcium, magnesium and vitamin D contents) (Mostafai et al.,
2019). In addition, the semi-solid structure and viscosity may contribute
to enhance these properties (Panahi et al., 2018). The main beneficial effects
associated with yogurt consumption are shown in Fig. 1.

2.1.1 Balance of the intestinal microbiota


The main mechanisms of action associated to yogurt consumption are pres-
ented in Fig. 2. The microorganisms of the starter culture can survive to the
gastrointestinal conditions and reach the gut. However, these microorganisms
Dairy foods and positive impact on the consumer’s health 99

YOGURT

Balance of Body Lactose Cancer


intestinal composition intolerance
microbiota

Prevention of colonization of Reduction in body mass Lower lactose content Inhibition of tumor cells
pathogens index (BMI) Production of β- Destruction of
Vitamin and enzyme Decreased waist galactosidase (product carcinogenic substances
synthesis circumference and small intestine)
Stimulation of the immune Lower percentage of
system body fat
Improved glycemic profile

Cardiovascular Bone structure Immune system


disease and integrity

Improvement Improvement in bone Production of antibodies


in lipid profile integrity Increased activity of the
Reduction in Reduction in bone loss macrophages
serum Lower fracture risk Improvement of the
cholesterol Higher bone intestinal barrier
mineralization

Fig. 1 Health effects associated to yogurt consumption. Images: Freepik.

Increased Acid production Inhibition of


beneficial Bacteriocins pathogenic
microbiota Antimicrobial components microbiota
Increased intestinal peristalsis
Competition for nutrients and
adhesion sites
Stimulation of the
antipathogenic defense

Fig. 2 Mechanisms of action in the inhibition of pathogenic microbiota.

are considered transients or visitors; therefore, they generally do not colonize


or persist for a long time at this site, suggesting that the regular consumption of
yogurts is mandatory (Donovan & Hutkins, 2018).
The consumption of yogurts, mainly with probiotic addition, can
increase the number of beneficial microorganisms in the intestine and inhibit
the growth of putrefactive or pathogenic bacteria. The end products of the
metabolism of beneficial bacteria, such as acids, decrease the pH of the colon
100 Silvani Verruck et al.

to values below those that pathogens can compete effectively. In addition,


these bacteria can excrete natural antimicrobial compounds (bacteriocins)
or other components (hydrogen peroxide, diacetyl, acetaldehyde, and
peptides), which can act as antimicrobial agents and inhibit the growth of
pathogenic bacteria (Uriot et al., 2017). Bacteriocins and some peptides
increase the membrane permeability of the pathogenic microorganism cells,
resulting in depolarization of the membrane potential and microbial
death. Hydrogen peroxide causes oxidation of sulfhydryl groups, leading
to enzyme denaturation, peroxidation of membrane lipids, increased
membrane permeability and cell death (Kerry et al., 2018). The organic acids
increase the intestinal peristalsis, and indirectly remove the pathogenic
microorganisms by accelerating their transit in the intestine (Fernandez,
Picard-Deland, Le Barz, Daniel, & Marette, 2017). Finally, there is compe-
tition for nutrients and adhesion sites between beneficial and pathogenic
microorganisms (Chandan et al., 2017).
The beneficial microorganisms can also stimulate the antipathogenic
defense of the host by activating or stimulating a pathway related to the
production of defensins. They are cationic antimicrobial peptides produced
in different cell types, such as Paneth cells in the crypts of the small intestine
and intestinal epithelial cells (Kerry et al., 2018).

2.1.2 Body composition and metabolic profile


Yogurt consumption may lead to a reduction in body mass index
(BMI), waist circumference, and percentage of body fat. Furthermore, it
can improve the glycemic profile of the consumers (Panahi et al., 2018).
The mechanisms of action on body composition are presented in Fig. 3.
The calcium content in yogurt plays an important role in regulating body
weight and metabolism by reducing lipogenesis and stimulating lipolysis
and lipid oxidation (Dugan & Fernandez, 2017). This effect is related to
the modulation of plasma 1,25-hydroxyvitamin D concentrations via
parathyroid hormone (PTH), which can increase the renal calcium reabsorp-
tion, enhance bone resorption and activate the kidney hydroxylase enzyme
(converts inactive vitamin D in active vitamin D). A high concentration of
calcium in the plasma decreases the synthesis of 1,25-hydroxyvitamin D,
resulting in a lower influx of calcium ions into the adipocytes. Therefore,
there is decreased intracellular calcium, reducing the activation of the gene
transcription of fatty acid synthase (FAS) within the adipocyte. Consequently,
there is an increase in lipolysis and decrease of de novo lipogenesis, mitigating
adiposity (Dugan & Fernandez, 2017).
Dairy foods and positive impact on the consumer’s health 101

Reduction of lipogenesis
Ca Stimulation of lipolysis
Increased lipid oxidation

Healthier body Suppression of food consumption


composition Protein
and Increased satiety
peptides Stimulation of mechanisms known
as signs of satisfaction and satiety
Glycemic control

Energy uptake
Appetite regulation

Insoluble compounds
Ca Fatty
Excretion in feces
acids

Healthier lipid Interruption of enterohepatic


profile Ca Bile salts circulation
Removal of circulating
cholesterol

Synthesis of deconjugated bile acids


Cholesterol is used in de novo
synthesis of bile acids
Reduced level of serum cholesterol

Fig. 3 Mechanisms of action in the body composition and lipid profile. Images: Freepik.

Proteins can regulate body weight due to suppression of food consump-


tion, increased satiety and stimulation of mechanisms known as signals of
satisfaction and satiety. The presence of viable microorganisms and products
of their metabolism can alter the colonic microbiota by modulating the
amount of energy uptake and the appetite (Fernandez et al., 2017).
The improvement of the metabolic health is related to the presence
of proteins and peptides in yogurt, which can control glycemia due to the
stimulation of gastrointestinal hormones, such as glucagon-like peptide-1
(GLP-1) and peptide proline-tyrosine-tyrosine (PYY). In addition, they play
an important role in the modulation of blood lipids and blood pressure.

2.1.3 Cardiovascular diseases and serum cholesterol


The consumption of yogurt, in combination with a healthy diet, may
result in reduced risk of cardiovascular disease, mainly due to the changes
in the lipid profile. The proposed mechanisms of action are presented in
Fig. 3. Saturated fatty acids can bind to calcium and form insoluble com-
pounds, which are excreted in the feces. Calcium can also bind to bile salts,
102 Silvani Verruck et al.

resulting in interruption of enterohepatic circulation and removal of


circulating cholesterol (Dugan & Fernandez, 2017). The presence of
beneficial microorganisms in the colon is associated with increased synthesis
of deconjugated bile acids, which are not fully absorbed by the colonic
microbiota and co-precipitate together with cholesterol, being excreted
in the feces. In addition, they could deconjugate bile acids to free acids,
which are excreted rapidly from the gastrointestinal tract. Thus, cholesterol
is used in the de novo synthesis of bile acids, reducing the serum cholesterol
level (Fernandez et al., 2017).

2.1.4 Lactose intolerance


Lactose intolerance is a condition observed in individuals unable to
hydrolyze the major milk carbohydrate (lactose) to its monosaccharides
(glucose and galactose), due to the absence of β-D-galactosidase enzyme
in the brush borders of the epithelial cells of the small intestine. Lactose
passes intact through the gastrointestinal tract and reach the intestine. Then,
it is fermented by the microbiota with production of organic acids, methane,
hydrogen and carbon dioxide. The presence of these metabolites and the
osmotically driven excessive water drawn into the intestine results in the
observed effects: abdominal pain, diarrhea, flatulence, bloating and cramps
(Chandan et al., 2017). Lactose intolerance can be caused by a congenital
deficiency, intestinal diseases, genetics or ethnic factors (Fernandez
et al., 2017).
The acid-lactic bacteria used as starter cultures in yogurts may improve
lactose intolerance. Mechanisms of action include: decreased lactose content
in the yogurts, and increased β-D-galactosidase enzyme activity in the
product or intestine (Pimenta et al., 2018). During the fermentation process,
there is consumption of 20–30% of the lactose present in milk, with the
production of lactic acid. Thus, yogurts present lower lactose content
than other unfermented dairy products (Fernandez et al., 2017). The micro-
organisms of the starter culture, mainly S. thermophilus, can produce β-D-
galactosidase in the small intestine and its activity is protected due to the high
buffering capacity of the products (Uriot et al., 2017).

2.1.5 Bone structure and integrity


The contents of calcium, phosphorus, protein, and micronutrient of yogurt
play an important role in the control of bone homeostasis. The yogurts
present a higher concentration of these components than milk, due to the
enrichment of the total solids, mainly with skimmed milk powder, to obtain
Dairy foods and positive impact on the consumer’s health 103

desirable texture characteristics. Peptides released by casein breakdown dur-


ing milk fermentation may accelerate the uptake of minerals (Chandan et al.,
2017). In addition, lactic acid plays an important role in increasing the
calcium content in the bones and strengthening them, as the acidic environ-
ment converts colloidal calcium into its ionic form, allowing its transport
to the cells of the intestinal mucosa and improving bone mineralization
(Chandan et al., 2017).
The consumption of yogurt is associated with improvements in bone
integrity and reduction of bone loss in elderly, reducing the risk of fracture.
The effect of bone mineralization is associated with the formation of
hydroxyapatite crystals and modulated by an interaction with the vitamin
D receptor genotype (Rizzoli & Biver, 2017). The amount of protein
ingested influences bone growth and accumulation of bone mass. Low
consumption of yogurts and dairy products during childhood and adoles-
cence can result in smaller stature and lower bone mineral mass, either
at specific sites or throughout the body, increasing the risk of fracture
(Rizzoli & Biver, 2017).

2.1.6 Immune system and related diseases


There are several mechanisms of action associated with the effect of yogurt
consumption on immune system enhancement, which are presented in
Fig. 4. The mechanisms include: (1) alteration of the metabolism of the
intestinal microbiota by increasing or reducing enzyme activity; (2) suppres-
sion of pathogenic microorganisms by the production of compounds with

Cytokines production
Immunoglobulin A production

Production of antibodies
Immune system Increased activity of the
macrophages

Alteration on the enzymatic activity


Inhibition of pathogenic microbiota
Physical barrier (EPS)

Fig. 4 Mechanisms of action in the immune system. Images: Freepik.


104 Silvani Verruck et al.

antimicrobial activity or competition for adhesion sites and nutrients; (3)


stimulation of immune systems by the production of antibodies or increase
of the activity of the macrophages; and (4) improvement of the intestinal
barrier.
The high permeability of the intestinal barrier is associated with several
diseases, such as infections, celiac disease, Chron’s disease and type 1 diabetes
(Uriot et al., 2017). Yogurt consumption could improve intestinal barrier
property, due to the higher production of the cytokines IL-6 and INFγ,
Immunoglobulin A (IgA), and IL-10 regulatory cytokine (Balcells,
Mariani, Weill, Perdigon, & Maldonado Galdeano, 2017; Pimenta et al.,
2018). In addition, the starter culture, especially S. thermophilus, could
secrete exopolysaccharides (EPS), which can create a mechanical barrier
in the intestine, reducing the permeability (Uriot et al., 2017).

2.1.7 Cancer
The anticarcinogenic effect of yogurt consumption is mainly related to
the presence of the starter culture microorganisms and could be divided
into four categories: (1) alteration of the intestinal microbiota composition,
(2) suppression of enzyme-producing bacteria, (3) inhibition of tumor cells,
and/or (4) destruction of carcinogenic substances (Pimenta et al., 2018).
The alteration of the composition of the microbiota by increasing the
number of beneficial microorganisms’ results in the production of beneficial
metabolites, such as butyrate, capable of stimulating apoptosis of cancer cells
and it is the energetic source preferred by colonocytes. In addition, there is
an alteration of the colonic metabolism to saccharolytic fermentations in
detriment of the proteolytic fermentations, resulting in more benign end
products. Finally, there is normalization of intestinal permeability, resulting
in prevention or delay in the absorption of toxins and strengthening of the
intestinal barrier mechanisms.
Suppression of enzyme-producing bacteria, such as those that produce
β-glucosidases, β-glucuronidases, and azoreductases, reduces the production
of carcinogenic metabolites. The enzyme β-glucuronidase can hydrolyze
compounds and release aglycones with carcinogenic activity. Azoreductases
and nitroreductases help in the formation of aromatic amines, compounds
that are harmful to human health (Pimenta et al., 2018).

2.1.8 General aspects


The consumption of yogurt can improve the well-being and reduce the risk
of diseases. More in-depth studies, preferably in vivo models and especially
Dairy foods and positive impact on the consumer’s health 105

through animal and clinical trials, need to be conducted to validate


epidemiological results before recommending the consumption of yogurt
to reduce the risk of specific diseases. In addition, it is necessary to evaluate
the effects of yogurts containing only the starter cultures (Fernandez et al.,
2017). Contradictory results are associated with the different strains of
L. bulgaricus and S. thermophilus used in the processing, the different
nutritional composition of the products, and the different diets and health
conditions of the individuals submitted to clinical trials.

2.2 Kefir
Kefir fermented milk can be produced using kefir grains or commercial
starter cultures. The Kefir grains are small masses with irregular shape,
gelatinous texture, and white to yellow color, resembling a miniature
cauliflower (Fig. 5A). The proximate composition of the grains is: 89–90%
moisture, 0.2% lipids, 3% proteins, 6% sugars, and 0.7% ash (Plessas et al.,
2017). Fig. 5B presents a scanning electron microscopy (SEM) micrograph
of Brazilian kefir grains.
Kefir grains present several microbial species, which are incorporated in
a polysaccharide matrix called kefiran (Amorim et al., 2019). The main
microorganisms found in Kefir grains are: lactic acid bacteria (108 CFU/g;
Cryptococcus, Lactobacillus, Lactococcus, Leuconostoc, Pediococcus, Streptococcus,
Tetragenococcus, Oenococcus), acetic acid bacteria (105 CFU/g; Acetobacter,
Gluconobacter), and yeast (107 CFU/g; Candida, Dekkera, Geotrichum,
Issatchenkia, Kazachstania, Kluyveromyces, Naumovozyma, Pichia, Saccharomyces,
Torulaspora, Zygosaccharomyces) (Bengoa, Iraporda, Garrote, & Abraham,
2019). However, the microorganisms present in the grains can vary according

Fig. 5 Kefir grains. (A) Macroscopic; (B) Microscopic aspects.


106 Silvani Verruck et al.

to the grain origin, type of milk used in the fermentation process, and meth-
odology of maintenance of the cultures (temperature, time, etc.) (Amorim
et al., 2019). Plessas et al. (2017) reported that the microbiota of Kefir grains
differs among countries. The kefir grains from Belgium, Ireland, and
Malaysia have Lactobacillus kefiranofaciens spp. and Lactobacillus kefiri as the
dominant cultures, while those from Brazil and China have Lactobacillus
helveticus, Lactobacillus casei and Lactobacillus kefiri.
The Kefir microorganisms co-exist in the grain in a symbiotic association
and have importance on the quality of the fermented milk. In the symbiotic
relationship, the growth of lactic acid bacteria results in the formation of
metabolic products, which are used by the yeasts. The yeasts produce amino
acids, vitamins, and other metabolites, which are used by the LAB (Rosa
et al., 2017). Considering the quality of the fermented milk, lactic acid
bacteria produce lactic acid, acetic acid, and antimicrobial compounds,
which contribute to the preservation of the product. Furthermore, they
can produce volatile compounds, which contribute to the sensory charac-
teristics. The yeasts produce carbon dioxide and ethanol, which contributes
to the effervescence, mouthfeel, and flavor of the products (Bengoa
et al., 2019).
Kefir fermented milk has a thick creamy consistency, mild acid taste and
mild aroma of fresh yeast; presenting natural effervescence and may contain
between 0.08% and 2% alcohol. It is usually produced using pasteurized cow
milk, but other types of milk can be used (such as buffalo, goat, and sheep),
as well as, whey (Bourrie, Willing, & Cotter, 2016). The traditional
methodology of producing Kefir fermented milk consists of inoculating
1–10% Kefir grains in milk at room temperature (25 °C) and ferment for
18–30 h. The grains are separated from the milk using sieves, and the
beverage is stored at 4 °C. Kefir grains can be reused in the manufacture
of new products, as they remain stable for long periods and the microbiota
is renewed due to the symbiosis (Shen et al., 2018).
The health effects associated with Kefir consumption are different
depending on the type of product. In some studies, Kefir fermented milks
produced using commercial starters presented a reduced effect compared
to the products produced using Kefir grains (Bourrie, Cotter, & Willing,
2018). This could be related to the differences in the microbiota, as commer-
cial starter cultures have a lower number of LAB and yeasts (Guzel-Seydim,
Dibekci, Cagdas, & Seydim, 2016). Fig. 6 presents some health effects
associated with Kefir fermented milk consumption.
Dairy foods and positive impact on the consumer’s health 107

Antimicrobial Immunomodulatory

ALLERGY

Anti-Allergenic
Gastrointestinal health
Anti-carcinogenic

Cholesterol metabolism Anti-hypertensive

Fig. 6 Health effects associated to Kefir fermented milk consumption. Adapted from:
Bourrie, B. C., Willing, B. P., & Cotter, P. D. (2016). The microbiota and health promoting
characteristics of the fermented beverage kefir. Frontiers in Microbiology, 7, 647. Images:
Freepik.

Considering the health effects associated to the consumption of Kefir


fermented milk, some of them have similar mechanisms of action to those
discussed for yogurt, like reduction in the lactose intolerance, antimicrobial
activity, effect on the gastrointestinal health, immunomodulatory properties,
body composition, and cholesterol metabolism. This is because the effects
are related to the presence of beneficial microorganisms or the metabolites
produced during fermentation, which are found in both products.
Table 1 reports studies that evaluated the health effects of the consump-
tion of Kefir fermented milks. The antimicrobial effect is associated to
the acids, hydrogen peroxide, carbon dioxide, acetaldehyde, kefiran and
bacteriocins produced by the microbiota ( John & Deeseenthum, 2015).
Furthermore, some lactobacilli found in Kefir grains have S-layer proteins,
which can align in unit cells of prokaryotic microorganisms, inhibiting their
Table 1 Health effects of Kefir fermented milks.
Attribute Study Product Results Conclusion References
Hypertension Male Wistar rats, Kefir fermented 37-mmHg reduction in systolic Kefir has anti- Amorim et al.
hypertensives, treatment milk, 4% grains, arterial pressure hypertensive effects and (2019)
was administered by gavage fermentation at 19% inhibition of angiotensin- is capable of inhibiting
over 21 days, at doses of room temperature converting enzyme (ACE) activity ACE activity in vivo
0.3 mL/100 g for 24 h
Metabolic 8-week old wild type Kefir fermented Decrease in weight gain and plasma Traditional kefir has the Bourrie et al.
syndrome C57BL/6 female mice, oral milk, 2% grains, cholesterol levels in traditional Kefir potential for improving (2018)
gavage of 100 μL of either fermentation at Lower liver triglycerides (one metabolic dysfunction
kefir (with traditional or 22 °C for 18 h traditional kefir) associated with obesity
commercial cultures) or
milk (control groups)
Daily for 12 weeks
Intestinal Male BALB-c mice Kefir fermented Increase in lactic acid bacteria Kefir consumption Erdogan,
microbial weighing between 20 and milk, 2% grains, Microorganisms survived the improved the microbial Ozarslan, Seydim,
population 25 g; 0.3 mL kefir/day for fermentation at gastrointestinal tract and population of the GIT and Tas (2018)
15 days 22 °C for 22 h reached the fecal area
Obesity Male C57BL/6mice, Kefir fermented Lower body weight and Kefir consumption Kim et al. (2017)
0.2 mL of kefir milk for milk, 1% grains, histopathological liver lesion score modulates gut
12 weeks fermentation at More Lactobacillus/Lactococcus, total microbiota and
25 °C for 24 h yeast and Candida mycobiota in High-
Up-regulation of the genes related to Fat-diet-fed mice,
fatty acid oxidation, PPARα, and which prevents obesity
AOX, in both the liver and adipose and NAFLD via
tissue promoting fatty acid
The plasma concentration of IL-6, a oxidation
proinflammatory marker, was
significantly reduced
Cancer Female BALB-c mice Kefir fermented The aberrant crypt foci were Kefir treatment may Melo, Mendonça,
(Mus musculus domesticus) milk, 2% grains, attenuated by approximately 43% contribute to and de Mendonça
(4-weeksold, 18  3 g), fermentation at (height) and 20% (width) in the kefir prevent and control the Rosa-Castro
5 mL/kg b.w. of UHT 24 h 24 °C for 24 h group growth of intestinal (2018)
fermented kefir milk by neoplastic cells
oral administration once
Daily for 8 weeks
Osteoporosis Twelve-week-old female Kefir fermented Reduction on the levels of C-terminal Kefir has potential to be Chen et al. (2015)
Sprague-Dawley (SD) rats, milk, 2% grains, telopeptides of type I collagen (CTx), an alternative treatment
164, 328 and 656 mg/kg fermentation at trabecular separation (Tb. Sp.) and for postmenopausal
BW/day 20 °C for 20 h bone turnover markers osteoporosis
Increase in trabecular bone mineral
density (BMD), trabecular thickness
(Tb. Th), bone volume (BV/TV),
trabecular number (Tb. N), and the
biomechanical properties (hardness
and modulus) of the distal femur
Increased intracellular calcium uptake
in Caco-2 cell
Constipation Twenty consecutive Not available Increase in stool frequency, Kefir improves bowel Turan, Dedeli,
patients, 500 mL/day for improvement in stool consistency and satisfaction scores and Bor, and İlter
4 weeks decrease in the consumption of accelerates colonic (2014)
laxative transit
Acceleration of the colonic transit
Improvement on the bowel
satisfaction scores
110 Silvani Verruck et al.

growth (Prado et al., 2015). The ability to reduce the cholesterol level in the
blood is associated with the presence of microorganisms with significant
levels of bile salt hydrolase (BSH) activity. This enzyme deconjugates bile
salts, which are less soluble and have less reabsorption from the intestinal
lumen, increasing their excretion. In this way, cholesterol is used to synthe-
size new bile salts (Bourrie et al., 2016). The effect of kefir consumption on
body composition and obesity is related to the changes in the gut microbiota.
The increase in the population of LAB (Lactococcus and Lactobacillus)
and yeasts induces the up-regulation of PPARα and promotes the lipid
oxidation. Furthermore, it decreases the inflammation and serum cholesterol.
These improvements can ameliorate obesity and fatty liver disease, resulting
in lower weight gain and hepatic lesions (Kim et al., 2017).

2.2.1 Diabetes mellitus


Diabetes Mellitus (DM) is a metabolic disorder characterized by chronic
hyperglycemia, resulting from a deficiency in the production or action of
the pancreatic hormone insulin. DM can be classified according to the
etiology, in type 1 (DM1), type 2 (DM2), gestational (GDM) or specific
(due to other causes). Recently, some authors have proposed a new condi-
tion, DM3, a neuroendocrine disorder characterized by the progression of
central insulin resistance to Alzheimer’s disease (Marques, Alves, Lee, & dos
Santos Quaresma, 2019).
There are some mechanistic hypotheses to explain the positive results
on the DM after kefir consumption:
1. The bioactive exopolysaccharides (EPS) produced by the micro-
organisms of the Kefir appear to trigger a cascade process, resulting in
increased release of insulin by pancreatic β-cells and increased glucose
uptake by cells and peripheral tissues (Marques et al., 2019). EPS appears
to activate glucagon hormone (which is similar to peptide 1 (GLP-1)),
gastric inhibitory peptide (GIP), and adenylate cyclase via cyclic adeno-
sine monophosphate (c-AMP), sensitization of Ca2+ ions and activation
of protein kinase A. In this way, there is an increase in the release of
insulin from pancreatic β-cells. Therefore, the increase of c-AMP in
pancreatic cells seems to contribute to a better secretion of insulin by
β-cells (Marques et al., 2019);
2. There is a reduction of oxidative stress, as kefir decreases the levels
of lipid peroxidation in the blood. It is well-known that peroxide
molecules can affect the production of proinflammatory cytokines, such
as IL-1, IL-6, and TNFα. These interleukins impair the insulin signaling
Dairy foods and positive impact on the consumer’s health 111

pathway by activating a recognized pro-inflammatory pathway that


promotes the dissociation of IkB/NF-kB, leading to pancreatic β-cell
damage and apoptosis ( Judiono et al., 2014).

2.2.2 Colon cancer


Colon cancer is the type of cancer with the highest mortality and morbidity,
being considered the fourth most common cancer type in men and the
third in women. Some bacteria can attach to the epithelium surface due
to the presence of a special protein structure. In this case, there is a stress
in the cell at the attachment point, resulting in a mutant cell division and
generation of cancer tissues and ulcerative colitis in the intestinal tissues.
The attachment allows other pathogens to bind to the surface, causing
aggregation (Guzel-Seydim et al., 2016).
There are some mechanistic hypotheses to explain the positive results in
the reduction of the risk of colon cancer after kefir consumption: (1) the
microorganisms present in the kefir can attach to the epithelium cells surface,
precluding the attachment by pathogenic bacteria; (2) the microorganisms
present in the kefir produce antimicrobial compounds, which can cause
the pathogens death; (3) the microorganisms present in kefir compete with
the pathogenic microorganisms for nutrients (Guzel-Seydim et al., 2016).
Furthermore, kefir consumption is associated to the decrease in tumor
growth due to: (1) antiproliferative effect on the cancer cells, (2) antioxidant
activity, (3) inhibition of enzymes that convert procarcinogenic compounds
in carcinogenic compounds, (4) increase in the apoptosis of the cancer
cells, (5) immunomodulatory properties, and (6) binding of mutagenic
compounds (Kesenkaş, G€ €
ursoy, & Ozbaş, 2017). The apoptosis of the
cancer cells can be related to: (1) the decrease in the secretion of TGF-α,
TGF-β, and Bcl2 and increase in Bax leading induced by kefir; (2) ROS-
mediated apoptosis induced by the bioactive peptides. The antiproliferative
effect on the cancer cells is related to the lower secretion of TGF-α and TGF-
β. Furthermore, an antiproliferative cytokine, named interferon-β, is secreted
in higher quantities by sphingomyelins presented in Kefir (Sharifi et al.,
2017). Kefiran can stimulate the immune system through T-cell activity
( John & Deeseenthum, 2015).

2.2.3 Hypertension
The anti-hypertensive effect of Kefir fermented milk consumption can be
related to the: (1) decrease in the generation of reactive oxygen species
(ROS), (2) improvement in the baroreflex sensitivity, and (3) inhibition
112 Silvani Verruck et al.

of angiotensin-converting enzyme (ACE) (Pimenta et al., 2018). The inhi-


bition of ACE is associated to the production of bioactive peptides during
the fermentation of milk by the microorganisms of the kefir grains, which:
(1) inhibit the formation of vasoconstrictor angiotensin I and aldosterone.
The aldosterone is a hormone associated to the stimulation of the increase
of Na in the serum, resulting in the increase in the blood pressure; (2) inhibit
the breakdown of bradykinin, a vasodilator hormone, decreasing the BP
(Rosa et al., 2017).

2.2.4 Metabolic syndrome


Metabolic syndrome (MetS) is characterized by anthropometric and physi-
ological abnormalities, resulting in high glucose level, hypertension, obesity,
high triglycerides, and low levels of high-density lipoprotein-cholesterol
(HDL-c). MetS is considered on the most contributors to the development
of type 2 diabetes and other conditions, such as hyperuricemia, gout,
mild kidney disease, oxidative stress, chronic inflammation and endothelial
dysfunction (Rosa et al., 2016). During fermentation of Kefir there is
production of bioactive peptides, which can reduce the risk of metabolic
syndrome and its derived complications by many mechanisms, such as:
(1) regulation of the levels of insulin, (2) regulation of blood pressure,
(3) satiety response; (4) uptake of free radicals, and (5) improvement in
the lipid profile (Ricci-Cabello, Olalla Herrera, & Artacho, 2012).
Therefore, the effect of Kefir fermented milk consumption on metabolic
syndrome is related to the effects on obesity, lipid metabolism, hypertension,
and diabetes, which were previously discussed in this chapter.

3. Cheese
Cheese is a rich source of essential nutrients such as proteins, lipids,
vitamins and minerals that performs an integral part of a healthy diet
(Silva et al., 2017). Cheese is defined as a fresh or matured product obtained
from milk coagulation, easily digestible and rich in nutritional components.
Cheese can be classified based on the type of milk used, manufacturing
process, fat content, type of fermentation, and its microbiota (Santiago-López
et al., 2018).
Cheeses are usually categorized as a dairy product with high fat content;
however, several correlation studies find no correlation between cheeses
consumption and cardiovascular diseases. The original purpose of cheese
Dairy foods and positive impact on the consumer’s health 113

making was to process milk into a stable and storable product. Today,
the consumption of cheese is mainly based on pleasure, and it contributes
with essential nutrients. Therefore, it is important to stress if it is safe to
eat regarding cardiovascular health (Hjerpsted & Tholstrup, 2016).
Concerning the nutritional benefits of cheese, the protein fraction of
cheese can act as a precursor of biologically active molecules. During cheese
ripening and food digestion, a large variety of peptides are released from milk
caseins. Some of these peptides are structurally similar to endogenous pep-
tides and, therefore, they can interact with receptors at the gastrointestinal
tract (for instance, opioid receptors), facilitate mineral absorption (CPPs), or
being absorbed and reach the bloodstream. Although the amount of food
derived peptides absorbed after oral ingestion can be low, there is increasing
evidence being built in clinical studies of several biological effects related
with the ingestion of some of these sequences (Santiago-López et al.,
2018; Silva, Balthazar, Rocha, et al., 2018).
During cheese ripening, casein is hydrolyzed into a large variety of
peptides by proteases and peptidases from milk, rennet, starter culture,
and secondary microbial flora. Some of these peptides are structurally similar
to endogenous peptides that play a crucial role in the organism as hormones
or antibiotics. These peptides generated during ripening can survive gastro-
intestinal digestion or serve as precursors from the final peptide form that
could interact with the same receptors than endogenous peptides and exert
agonistic or antagonistic effects in the organism (López-Expósito, Amigo, &
Recio, 2012). The ripening step of cheese making provides bioactive
compounds such as: peptides, exopolysaccharides, fatty acids, organic acids,
vitamins, aminobutyric acid (GABA), and CLA. Some of these compounds
could inhibit angiotensin-converting enzyme (ACE) and exhibit anti-
oxidant, antimicrobial, antiproliferative activities and anti-hypertensive
activity. The bioactivities lead to health-protective effects associated with
a reduced incidence of cardiovascular disease risk factors, such as obesity,
dyslipidemia, and type 2 diabetes, as well as reduced incidence of metabolic
syndrome (Santiago-López et al., 2018).

3.1 Nutritional value of cheese


Cheese contains a high concentration of essential nutrients relative to its
energy level. Its precise nutrient content is influenced by the type of milk
used, the manufacturing process, and the ripening time, as cheese compo-
sition in fresh, soft, semi-hard, and hard cheese varies (Vacca et al., 2018).
114 Silvani Verruck et al.

Most of the lactose from milk is lost in whey during cheese manufacture, and
the residual lactose in cheese curd is usually fermented to lactic acid by the
starter bacteria. With the exception of fresh cheeses, most cheeses are
lactose-free or contain only trace amounts of this component. Thus, cheeses
can be consumed without ill effects by lactose-intolerant individuals
(Szilagyi & Ishayek, 2018).

3.1.1 Fat content


The fat content of cheese depends on the milk used, the method of
manufacture and the type of cheese manufactured. From a nutritional point
of view, the digestibility of fat in different varieties of cheese is in the range of
88–94% (Trancoso-Reyes, Gutierrez-Mendez, Sepulveda, & Hernández-
Ochoa, 2014). Cheese fat generally contains approximately 66% saturated
fatty acids (SFA), which palmitic acid represents 57.4%, followed by myristic
(21.6%) and stearic (17.6%), 30% monounsaturated fatty acids (MUFA), and
4% polyunsaturated fatty acids (PUFA) (Hickey et al., 2018). Therefore,
cheese represents a significant dietary source of total fat and SFA.
Due to some negative evidence, SFAs are seen as bad for health,
influencing cholesterol level in blood lipids. Total plasma cholesterol-raising
effects of SFAs are generally greater with medium chain lengths (lauric
C12:0, myristic C14:0, and palmitic C16:0) than for those with longer chain
lengths (stearic acid C18:0) (Maki, Eren, Cassens, Dicklin, & Davidson,
2018). In addition, stearic acid, which is an important component of the
SFAs in cheese, is rapidly converted to the MUFA oleic acid C18:1, which
is considered to be one of the healthier sources of fat in the diet and is not
related with cardiovascular risk. It is important to note that some SFA plays
an important role in cell regulation by protein acetylation, in gene expres-
sion as well as in the modulation of genetic regulation, in the regulation
of the bioavailability of PUFA, and fat deposition (Markey et al., 2017).
As well, it is known that butyric acid may play a role in cancer prevention,
caprylic and capric acids have antiviral activities, and lauric acid may have
antiviral, antibacterial, and anti-cariogenic properties (Huang et al., 2014).
The cholesterol content of cheese comes from milk fat and ranges from
approximately 10 to 100 mg/100 g depending on the variety. In addition,
dietary cholesterol has much less influence on blood cholesterol level than
dietary saturated fat (Manuelian, Currò, Penasa, Cassandro, & De Marchi,
2017). Dietary cholesterol is important for the human body as a precursor
for cell membranes, bile salts, and steroid hormones that are essential for life.
Studies related 100 mg cholesterol per day as a healthy dietary consumption
Dairy foods and positive impact on the consumer’s health 115

(Pang et al., 2017). Furthermore, as it happens with the SFA, dietary


cholesterol not only raises atherogenic LDL but also raises the antiatherogenic
HDL cholesterol (Maki et al., 2018), when evaluating atherogenic and
thrombogenic indices in dairy products (Balthazar et al., 2016).
Fatty acids participate in various biological processes, serving as energy
substrates and regulating cells, as well as influencing gene expression, PUFA
bioavailability, and fat deposition. In addition, fatty acids may play a role in
cancer prevention (Santiago-López et al., 2018).
Conjugated linoleic acid is naturally found in milk and is formed as a
result of incomplete biohydrogenation of dietary fatty acids in the cow’s
rumen. Generally, dietary lipids are rapidly hydrolyzed in the rumen, and
the resulting free PUFA are subjected to biohydrogenation by microorgan-
isms. Consequently, one part is absorbed by the rumen and another in the
gastrointestinal tract, thereby incorporating CLA into mammary glands and
milk fat (Chin, Liu, Storkson, Ha, & Pariza, 1992). Other factors involved in
the subsequent formation of CLA in cheeses are the processing conditions,
the raw milk composition, and prior fermentation time (Santiago-López
et al., 2018). CLA has been reported to have several beneficial effects in
health-related disorders when tested in vitro and in animal models, including
anti-carcinogenic, anti-adipogenic, anti-atherogenic, anti-diabetogenic,
and anti-inflammatory properties (Mohan, Anand, Kalscheur, Hassan, &
Hippen, 2013).

3.1.2 Minerals and vitamins content


Most of the fat-soluble vitamins in milk are retained in cheese fat. The
concentration of water-soluble vitamins in cheese is generally lower than
in milk due to the losses in the whey. A greater concentration of fat-soluble
vitamins, rather than water-soluble vitamins, is found in cheese because
whey is removed during the manufacturing process. The main vitamins pre-
sent in cheese are riboflavin, vitamin B12, niacin, folate, and vitamin
A (Santiago-López et al., 2018). For instance, 50 g of Cheddar cheese can
provide 28% and 32% of the recommended daily intake of vitamin A for
men and women, respectively. This is especially important because vitamin
A has various biological functions, such as stimulating the immune system,
regulating gene expression, and sustaining lowlight vision (Medeiros
et al., 2018).
Cheese is also an important source of several minerals, in particular,
calcium (Ca), zinc (Zn), phosphorus (P), and magnesium (Mg). Ca and P levels
in cheese are much higher than in milk: four to five times in soft cheeses,
116 Silvani Verruck et al.

seven to eight times in semi-hard cheeses, and up to 10 times in hard cheese.


Actually, a 50-g serving of hard cheese provides approximately 400 mg
Ca which covers almost 100% of the recommended daily intake of Ca in
children between 1 and 10 years old. Furthermore, the Ca/P ratio is
particularly useful to the body, as it is digested in a form that is highly
bio-available because of the complexes that are formed between Ca and
the casein peptides within cheese. Such complexes maintain Ca in a soluble
form and protect the Ca against precipitation in the intestine, facilitating Ca
absorption. As cheese is a concentrated source of bio-available Ca, increasing
the amount consumed in the daily diet together with a good source of
vitamin D has the potential to safeguard against osteoporosis in future,
particularly in those that consume inadequate quantities of Ca at a young
age (Silva, Balthazar, Rocha, et al., 2018). Dietary Ca could affect the body
fat mass by increasing fecal fat excretion as well as by stimulating lipolysis
and inhibiting lipogenesis (Castro Burbano, Fajardo Vanegas, Robles
Rodrı́guez, & Pazmiño Estevez, 2016). Furthermore, it has been demon-
strated that calcium had hypolipidemic mechanisms via inhibition of fat
absorption and increased fecal fat excretion, inhibition of the absorption
of bile acids, and a Ca-induced increase in the conversion of cholesterol
to bile acids (Chen et al., 2016).
Cheese contributes very little to dietary iron; however, a wide range of
sodium (Na) levels are found in cheese due to different amounts of salt added
during cheese making. Although there is considerable awareness about the
fact that Na intake contributes to hypertension, cheese adds only about
5–8% of total Na intake (Silva, Balthazar, Rocha, et al., 2018). Although
cheese suffers from an adverse image due to its fat and salt content, the
variety of cheeses with reduced fat or salt content available on the market
make possible to include this food in all kind of diets (Silva et al., 2018).

3.1.3 Protein content


Cheese contains a high content of biologically valuable protein, which
ranges between 4% (cream cheese) and 40% (Parmesan) depending upon
the variety. Also, the nutritional value of cheese proteins does not change
during cheese manufacturing, and the content tends to vary inversely with
the fat content (Gore, Mardon, Guerinon, & Lebecque, 2016). Cheese pro-
tein is almost digestible, as the ripening phase of cheese manufacture involves
a progressive breakdown of casein to water-soluble peptides, many of them
having bioactivity, and free amino acids. These peptides are only active
after they have been released from their parent protein by proteolysis and
Dairy foods and positive impact on the consumer’s health 117

can exert a wide range of activities such as antihypertensive, antioxidant,


antimicrobial, and immunomodulation (Silva, Balthazar, Esmerino, et al.,
2018). Among the amino acids content in cheese, it is important to highlight
the high lysine content. Lysine has a high bioavailability in cheese due to the
absence of Maillard reactions (Zhu et al., 2018).

3.1.4 Lactose content


Most of the lactose from milk is lost in whey during cheese manufacture,
and the residual lactose in cheese curd is usually fermented to lactic acid
by the starter bacteria. As well, lactic acid bacteria hydrolyze lactose during
fermentation and produce high concentrations of lactic acid and other
organic acids (Szilagyi & Ishayek, 2018).
With the exception of fresh cheeses, most cheeses are lactose free or
contain only trace amounts. Thus, cheeses can be consumed without ill
effects by lactose-intolerant individuals. Under normal dietary conditions,
about 30–40% of the calcium contained in milk and cheese is absorbed in
the gut either through vitamin D-dependent transport across the duode-
num, facilitated diffusion or under the influence of lactose in the distal small
intestine via the paracellular route. Thus, lactose in dairy foods can facilitate
intestinal calcium absorption (Ugidos-Rodrı́guez, Matallana-González, &
Sánchez-Mata, 2018). Also, most lactose intolerance individuals can tolerate
up to 12 g of lactose (250 mL of milk, representing 300 mg of calcium and
30% of recommended calcium intakes) without suffering gastrointestinal
symptoms, although symptoms become more prominent at doses above
12 g and are appreciable after 24 g of lactose (Rozenberg et al., 2016).
Lactose intolerance can prompt avoid all dairies, but this is not necessary
for most people. In particular, yogurt and hard cheese are well tolerated and
provide the nutritional benefits of dairy products (Szilagyi & Ishayek, 2018).

3.1.5 Bioactivity compounds


Table 2 shows the bioactive peptides from different types of cheese and their
functional effects in vitro. Hypertension affects up to an average of 30% of
the adult population in developed countries, and the relationship between
hypertension and coronary heart disease is well established (Prabhakaran
et al., 2017). The treatment of hypertension is no longer limited to the
simple prescription of pharmaceuticals. Dietary efforts to decrease saturated
fat and sodium and increase potassium, calcium and soluble fiber intake
affect blood pressure positively (Martyn-Nemeth et al., 2016). Although
proteins from several different foods have been identified as precursors of
118 Silvani Verruck et al.

Table 2 Bioactive peptides from different types of cheese and their functional effects
in vitro.
Cheese Bioactivity Conclusions References
Pecorino Romano, Antibacterial Large spectrum of Rizzello et al.
Canestrato gram-positive end (2005)
Pugliese, negative bacteria
Crescenza, Caprino inhibition of water-
del Piemonte, soluble fractions
Caciocavallo and (20–200 μg/mL)
Mozzarella
Australian Cheddar ACE- inhibition Dependent ripening Ong and Shah
time ACE-inhibitory (2008)
activity
Indian Cheddar Antioxidant Dependent ripening Gupta, Mann,
time ACE and Kumar, and
antiproliferative Sangwan
capacity (0–16.61 μmol (2009))
of Trolox/mg of
protein)
Asiago d’allevo ACE- inhibition Independent ripening Lignitto et al.
time ACE (2010)
Australian Cheddar Antioxidant, Antimicrobial, Pritchard,
antimicrobial, and antiproliferative, and Phillips, and
ACE-inhibitory ACC inhibitory activity Kailasapathy
was variety dependent (2010)
Japanese Antiproliferative Antiproliferative Yasuda et al.
Montagnard, Pont- capacity dependent on (2010)
l’eveque, variety
Brie, Camembert,
Danablue, and Blue
Brazilian Coalho Antioxidant, Antiproliferative Silva et al.
Cheese zinc-binding, capacity (2012)
and antimicrobial (1895–2221 μM
Trolox) and peptide
profile were variety
dependent
Feta, Roquefort, Antioxidant and Antiproliferative Meira et al.
and Pecorino ACE-inhibitory capacity and ACE- (2012)
inhibitory activity were
variety dependent
Mexican Cottage Antioxidant and Dependent ripening Abadı́a-Garcı́a
antilisterial time antiproliferative et al. (2013)
capacity
Dairy foods and positive impact on the consumer’s health 119

Table 2 Bioactive peptides from different types of cheese and their functional effects
in vitro.—cont’d
Cheese Bioactivity Conclusions References
Italian Parmigiano Antioxidant Antiproliferative Bottesini et al.
Reggiano capacity unaffected by (2013)
ripening time and
gastrointestinal
digestion
Spanish Antioxidant Antiproliferative Timón, Parra,
Burgos-type capacity and peptide Otte,
profile were rennet Broncano, and
dependent Petron (2014)
Italian Parmigiano ACE-inhibitory Antiproliferative Bernabucci,
Reggiano and capacity unaffected by Catalani,
Grana Padano gastrointestinal Basirico,
digestion Morera, and
Nardone
(2014)
Italian Stracchino Antioxidant Low cellular oxidative Pepe et al.
soft stress (2016)
Mexican fresh goat Antioxidant and High biological Hernandez-
cheese ACE-inhibitory activities with slight Galán et al.
differences associated (2017)
with distinct heat
treatments

antihypertensive peptides, milk proteins are the main source of this type
of bioactive peptides. Thus, antihypertensive peptides have been found in
processed dairy products, including several types of cheese (Santiago-
López et al., 2018).
Angiotensin-converting enzyme (ACE) plays a role in the renin-
angiotensin system by converting angiotensin I to a potent vasoconstrictor,
angiotensin II, which also induces the release of aldosterone and therefore
increases the sodium concentration and blood pressure. ACE also takes part
in the kinin–kallikrein system as it hydrolyzes bradykinin, which has a
vasodilator action (Yue et al., 2018). However, several of the food-derived
antihypertensive peptides may act by different mechanisms other than
inhibiting ACE such as direct vasodilator effects, antioxidant activity, or
by interaction with opioid receptors.
120 Silvani Verruck et al.

It is also important to highlight the lack of correlation found for some


peptides between the in vitro ACE-inhibitory activity and the antihyperten-
sive effect. This discrepancy can be due to their further degradation during
gastrointestinal digestion, the impossibility to reach the target organ in the
organism in a sufficient amount, or because other mechanisms different than
ACE inhibition may be involved. This fact has provided doubts regarding
the use of the in vitro ACE-inhibitory activity as the exclusive criteria to
identify potential antihypertensive peptides (Sun et al., 2017). Cheese is a
complex food matrix containing a large number of different peptides which
change with the ripening time. The identification of novel fragments with
ACE-inhibitory activity has been performed by several fractionation steps
and consequent evaluation of the activity (Tu et al., 2018).
There is almost no information considering the potential of cheese as
a source of antibacterial peptides that can be generated by hydrolysis of
milk proteins and can then even interact with microorganisms involved
in cheese processing. A higher degree of early proteolysis was related with
higher antioxidant activity, although it was also dependent on the starter
culture employed (Elbarbary, Ejima, & Sato, 2019).
Casein phosphopeptides (CPPs) are peptides with various degrees of
phosphorylation which are released in vitro and in vivo by enzymatic hydro-
lysis of the different casein fractions (Sun et al., 2018). Most CPPs contain
clusters of three phosphorylated serine residues followed by two glutamic
acid residues named the “phosphoserine cluster.” As well, the presence of
this anionic triplet (SerP-SerP-SerP-Glu-Glu) is a distinctive feature for
all functional CPPs, and these peptides have a high net negative charge,
binding divalent cations with the formation of soluble complexes (Kume,
Sasayama, Kaneko, Kurisaki, & Oda, 2013). The ability of CPPs to elicit
the optimal biological effects relies on the presence of Ca–CPP aggregates
in the appropriated conformation and concentration. Calcium divalent has
ions that may facilitate the organization of peptides in the aggregates. Thus,
the mechanism involved in the differences of iron absorption could be partly
explained by differences in protein composition that affect the accessibility
of iron–peptide complexes. Moreover, other non-phosphorylated residues
can also be involved in the binding and stability of the complexes formed
(Sun et al., 2018).
There are many enzymes common in cheese varieties. Nevertheless,
the peptide composition is unique for each cheese type and reflects a charac-
teristic ripening process. Therefore, CPPs could be regarded as transient
intermediate components in the cheese; they either accumulate or are
Dairy foods and positive impact on the consumer’s health 121

degraded by cheese enzymes to shorter peptides and free amino acids,


including SerP (Silva et al., 2016). Apart from the metal binding and anti-
cariogenic properties, CPPs have other bioactive properties such as antioxi-
dant, immune stimulatory, and influence on growth and differentiation of
osteoblastic cells (Reema, Lahiri, & Roy, 2014).
Regarding opioid peptides, these exert activity by binding to specific
receptors of the target cells in an agonistic or antagonistic fashion. Milk-
derived opioid peptides are characterized by the presence of a tyrosine
residue at the N-terminal and another aromatic amino acid at a third or
fourth position which is an important structural motif that fits into the
binding site of opioid receptors. Opioid receptor ligands are those termed
β-casomorphins derived from β-casein. The sequential action of several
digestive enzymes may be involved in the formation of β-casomorphins
(Santiago-López et al., 2018). There are also several studies indicating that
different cheeses contain peptides incorporating the β-casomorphin-7
sequence, which could act as precursors during further digestion processes
(Nguyen, Johnson, Busetti, & Solah, 2015).
With regard to cancer prevention, a considerable number of studies have
indicated anticarcinogenic properties in cheeses (Santiago-López et al.,
2018). By serving as an apoptotic inducer for tumor development, lacto-
ferrin and lactoferricin of bovine milk have been demonstrated to suppress
the growth of cancer cells in which DNA damage is involved in vitro and
in vivo (Freiburghaus, Janicke, Lindmark-Månsson, Oredsson, & Paulsson,
2009; Freiburghaus, Lindmark-Månsson, Paulsson, & Oredsson, 2012;
Henry & Alexis, 2009). It seems that in addition to a certain net positive
charge and hydrophobicity, the ability to adopt an amphipathic conforma-
tion is critical for antitumor activity. An amphiphilic and a positive net
charge are recognized as major structural motifs determining the interaction
with bacterial membranes, which has been accepted as a common target in
their mechanism of action (Shah et al., 2015).

4. Butter
Butter is known as a solid emulsion of fat globules, water, and air. It is
obtained by churning cream while inversion of the aqueous phase occurs,
forming the mass of the butter (Prudesncio et al., 2017). The fat content
in the butter is about 80%, which is partially crystallized and partly in
globular or liquid form. Worldwide butter can be found in the form of salted
122 Silvani Verruck et al.

butter, unsalted butter, pasteurized-cream butter, ripened-cream butter,


unripened-cream butter, sweet-cream butter, sour-cream butter, creamery
butter, and cold-storage butter (Mehta, 2009). Other popular products
obtained from butter are butter oil and ghee. Butter oil is obtained from
butter or cream fat-concentration through the removal of around 99% of
nonfat solids and water. Butter oil is also known as “milk fat,” “anhydrous
milk fat,” “dry butterfat,” and “dehydrated butterfat” (Mortensen, 2011a).
Ghee is traditionally produced in India and manufactured from cow’s or
buffalo’s milk butter. It has similarities with butter oil, but while butter oil
is obtained by centrifugation and vacuum dehydration, ghee is obtained
by heat-induced desiccation at a higher temperature (Mortensen, 2011a).
Triacylglycerols (around 98%) are the major fraction in butterfat,
followed by diacylglycerols (0.3%), monoacylglycerols (traces), phospho-
lipids (0.3%), sterols (0.3%), free fatty acids (FA) (0.1%) and traces of
waxes, squalenes and carotenoids (Frede, 2011). Recent new findings of the
nutritional significance of butterfat constituents associate their consumption
with several health benefits (Fig. 7). The anti-carcinogenic potential of
butterfat components, such as conjugated linoleic acids (CLA), sphingomyelin,
butyric acid, ether lipids, β-carotene, and vitamins A and D were reported
(Akalln & Tokusoglu, 2003; Jahreis et al., 1999; Khanal & Olson, 2004;
Parodi, 1999). The role of CLA and sphingomyelin in preventing cardiovas-
cular diseases and in immunomodulatory activity were also described

Fig. 7 Butterfat constituent’s association with health benefits. Images: Freepik.


Dairy foods and positive impact on the consumer’s health 123

(Cook & Pariza, 1998; MacDonald, 2000). The investigation on the benefits
of butter consumption and vitamins D and E to the bone formation showed
interesting outcomes (Christakos, Dhawan, Verstuyf, Verlinden, &
Carmeliet, 2016; Pimpin, Wu, Haskelberg, Del Gobbo, & Mozaffarian,
2016). All these health benefits are described below.

4.1 Beneficial health compounds in butter


4.1.1 Conjugated linoleic acids
Conjugated linoleic acids (CLA) are a group of naturally occurring 18-carbon
fatty acids, containing one or more double bonds in trans geometric config-
uration, that show bioactive effects on human health (Bauman, Tyburczy,
O’Donnell, & Lock, 2011). The predominant isomer in milk fat is the
cis-9, trans-11 CLA (75–90% of total CLA) followed by trans-7, cis-9 CLA
(5–10% of total CLA) (Bauman et al., 2011). Milk fat is the richest natural
dietary source of CLA, containing 2.4–28.1 mg/g, while in butter the CLA
content ranged from 5.5 to 6.5 mg/g fat (Chin et al., 1992; Lin, Boylston,
Chang, Luedecke, & Shultz, 1995; Parodi, 1997a). As CLA is formed by
hydrolysis of the ester linkages and biohydrogenation of polyunsaturated fatty
acids (PUFA) during fermentation in the rumen, the cis-9, trans-11-18: 2
isomeric form is also called rumenic acid (Bauman et al., 2011). The isomer
cis-9, trans-11-18:2 is related to anti-carcinogenic and anti-atherogenic
effects, while trans-10, cis-12 CLA is related to anti-carcinogenic, antiobesity
and anti-diabetogenic effects (Bauman et al., 2011).
Several studies investigated the role of CLA on a wide range of
carcinogenic cells lines, such as human malignant melanoma, colorectal,
breast, lung, prostate, and ovarian cancer (Parodi, 1997a, 1997b). The
mechanism of CLA action inhibition of carcinogenic cell lines is mainly
due to the modulation of apoptosis and cell cycle control (Ochoa et al.,
2004). This mechanism blocks the growth and metastatic spread of tumors
(Benjamin & Spener, 2009). CLA showed best antiproliferative effects
during in vitro studies in murine myeloid leukemia (Palombo, Ganguly,
Bistrian, & Menard, 2002) and human colorectal and prostate colorectal cells
(Chajes et al., 2003), as well as in human studies on breast (Chujo et al.,
2003; McCann et al., 2004) and prostate cancers (Ochoa et al., 2004).
Another research suggested an inverse association between CLA dietary
intake in postmenopausal women and the incidence of breast cancer
(Aro et al., 2000). In a clinical trial study with 24 women with resectable
invasive breast adenocarcinoma, the consumption of CLA during 12 days
before tumor resection decreased the S14 protein expression that resulted
124 Silvani Verruck et al.

in a reduction of proliferation index (McGowan et al., 2013). High S14


protein expression could be a metastasis prediction because this protein
mediates the induction of lipogenesis by progestin in breast cancer cells
and accelerates their growth (Kinlaw, Quinn, Wells, Roser-Jones, &
Moncur, 2006).
CLA may also play a beneficial role against coronary heart diseases.
Table 3 shows studies where human subjects consumed butter to investigate
its role in metabolic syndrome, mainly diabetes, coronary heart disease,
stroke, and cerebral infarction. CLA-fed rabbits with atherosclerosis
decreased ratios of the LDL: HDL cholesterol and total cholesterol to
HDL cholesterol (Benjamin & Spener, 2009). CLA is considered a potent
anti-atherogenic dietary fatty acid in an animal model (Naumann et al.,
2006; Weldon, Mitchell, Kelleher, Gibney, & Roche, 2004). The CLA
content in milk fat is strongly influenced by dietary effects and also by
physiological factors, dairy breed, stage of lactation, and parity, and other
individual animal variations (Bauman et al., 2011). Due to this characteristic,
the animal diet can be modified in order to improve the CLA contents in
milk fat. Desroches et al. (2005) compared the effects of the consumption
of a modified butter naturally enriched with CLA by the addition of
sunflower oil to the diet of dairy cows with the consumption of a control
butter that was low in CLA in obese men. The consumption of the enriched
CLA butter diet induced a decrease in plasma total cholesterol and the ratio
of total to HDL cholesterol. Haug et al. (2008) investigated the consumption
effect of butter naturally enriched in about 20 g cis-9, trans-11-CLA plus
vaccenic acid daily for 3 weeks in growing pigs. Their results showed an
increase of alpha-linolenic acid and a decrease of myristic and palmitic acid
in serum compared to pigs fed with control butter, implying a potential
benefit of the cis-9, trans-11-CLA plus vaccenic acid butter on serum fatty
acid composition. In diets that include two eggs/day with butter for
12 weeks, it was observed that blood cholesterol levels did not significantly
change in normocholesterolemic and hypercholesterolemic males (Flynn,
Nolph, Sun, Navidi, & Krause, 1991). A prospective study that evaluated
the effect of margarine (a source of trans fatty acids) and butter intake among
over 800 middle-aged men followed for 21 years showed no relation with
butter consumption and development of coronary heart disease (Gillman
et al., 1997).
CLA consumption also shows interesting outcomes in studies with
diabetes, obesity, immunomodulation, and osteosynthesis (bone formation)
(Benjamin & Spener, 2009; Pimpin et al., 2016). CLA supplementation in
Table 3 Consumption of butter and their role in metabolic syndrome, mainly diabetes, coronary heart disease, stroke, and cerebral infarction.
Age Time of
Disease outcome Sample size (years) study Main results References
Type II diabetes 4304 men and 40–69 23 years Butter had a weak effect on diabetes risk Montonen et al. (2005)
mellitus women
Cerebral infarction, 26,556 men 50–69 13.6 years There were no strong associations between intake Larsson et al. (2009)
intracerebral and (smokers) of butter and risk of any stroke subtype
subarachnoid
hemorrhage
Ischemic heart disease, 16,396 women and 44–74 12 years Statistically significant interactions between sex and Sonestedt et al. (2011)
stroke, and total 10,049 men butter consumption were not observed on incident
mortality cardiovascular disease
Ischemic heart disease, 120,852 men and 55–69 10 years A slightly increased risk of total mortality and Goldbohm, Chorus,
stroke, and total women ischemic heart disease was found for butter intake in Galindo, Schouten, and
mortality women van den Brandt (2011)
Cardiovascular disease 3630 adults <75 10 years Long-term butter intake is not associated with Aslibekyan, Campos,
adverse cardiovascular outcomes and Baylin (2012)
Coronary heart disease 751 men and 1008 50–93 16.2 years No association between intake of butter and Avalos et al. (2013)
women coronary heart disease was found
Type 2 diabetes mellitus 2091 men and 50–70 6 years The consumption of butter was associated with a Zong et al. (2014)
and cardiometabolic women significantly lower risk of type 2 diabetes and
traits favorable changes of cardiometabolic traits
Continued
Table 3 Consumption of butter and their role in metabolic syndrome, mainly diabetes, coronary heart disease, stroke, and cerebral infarction.—cont’d
Age Time of
Disease outcome Sample size (years) study Main results References
Mortality risk between 6384 persons with 35–70 8 years Intake of butter was related to an increased Sluik et al. (2014)
individuals with and diabetes and mortality risk for individuals with diabetes
without diabetes 258,911 without
diabetes
Type 2 diabetes mellitus 145,087 women 26–65 22 years Butter consumption showed nonsignificance Guasch-Ferre et al.
predicted risk estimates for diabetes occurrence, as (2015)
occurred with olive oil when the models were
adjusted for body mass index
Type 2 diabetes mellitus 16,428 women and 45–74 14 years Decreased risk of type 2 diabetes mellitus was seen Ericson et al. (2015)
10,502 men with higher intakes of butter in women
Type 2 diabetes mellitus 25,307 participants 23–74 12.3 years Within butter consumers, no relation with diabetes Buijsse et al. (2015)
was observed, while no consumers of butter
showed higher diabetes risk
Total mortality, cause- 2907 participants 65 22 years No significant associations of milk fat consumption Otto et al. (2018)
specific mortality, and (butter) and total incident cardiovascular disease,
cardiovascular disease coronary heart disease, or stroke were observed
Dairy foods and positive impact on the consumer’s health 127

the diet of people with diabetes, mainly type 2, can lead to better control of
serum glucose. This behavior is strongly related to the trans-10, cis-12-CLA
isomer bioactive effects in subjects with type 2 diabetes (Belury, Mahon, &
Banni, 2003). In another study, rats that ingested a high-fat diet containing
butter naturally enriched with cis-9, trans-11-CLA showed hyperinsulinemia
effects and increased their HDL cholesterol in comparison to control butter
ingestion (de Almeida et al., 2015). CLA may also play a beneficial role in
reducing body fat in laboratory mice, while body protein, water, and ash
increased their content (Park et al., 1997). The effects of CLA on body
composition appear to be due to the reduction of fat deposition and an
increase of lipolysis in adipocytes when tested in rats, pigs and cattle
(Azain, 2004). In addition, Penedo et al. (2013) studied the immunomod-
ulatory effects of a butter naturally enriched with cis-9, trans-11-CLA in
healthy young adults. Key inflammatory mediators often altered during
chronic sub-clinical inflammation were investigated. Their results showed
a decrease in the production of pro-inflammatory biomarkers associated
with overweight and obesity when butter naturally enriched with cis-9,
trans-11-CLA was ingested. Greater hepatic and systemic insulin sensitivity
and lower fat content in the liver are linked to glucose tolerance improved
by dairy fat consumption (Kratz et al., 2014). Therefore, CLA also reduces
the rate of bone resorption, improve bone formation and enhances calcium
absorption from the diet in adult rats (Kelly & Cashman, 2004).

4.1.2 Sphingolipids
Other functional components present in the butter are sphingolipids,
such as ceramides, sphingomyelin, cerebrosides, sulfatides, and gangliosides
(Hellgren & Nordby, 2017; Saxelin, Korpela, & Mayr€a-M€akinen, 2003).
Sphingolipids are found mainly in the milk fat globule membrane, however,
low-fat and nonfat as well as full-fat dairy products are good sources of these
compounds (Parodi, 1997a). Miller, Jarvis, and McBeanL (2000) reported
that sphingolipids influence cell regulation, and thus carcinogenesis and
tumor formation during in vitro and experimental studies. Other beneficial
effects of sphingolipids on human health are antimicrobial and immuno-
modulatory activities, as well as inhibition of cholesterol adsorption
(Akalin, Gonc, & Unal, 2006; Merrill et al., 1997; Possemiers, Van
Camp, Bolca, & Verstraete, 2005; Vesper et al., 1999). Sphingomyelin rep-
resents about one-third of total phospholipids in dairy fat (Lopez & Menard,
2011). When consumed, sphingomyelin is transformed to ceramide by
sphingomyelinase, and further ceramide is digested to sphingosine and a free
128 Silvani Verruck et al.

fatty acid before being absorbed (Nilsson, 2007). Ceramide is known as a


cancer cell apoptosis inducer (Birbes, Bawab, Obeid, & Hannun, 2002;
Hannun & Obeid, 1995). The consumption of sphingomyelin was related
to the prevention of colon cancer in mice and humans (Berra, Colombo,
Sottocornola, & Giacosa, 2002; Schmelz, Sullards, Dillehay, & Merrill,
2000). In addition, reduction of plasma cholesterol and triacylglycerol levels
and prevention of hepatic steatosis was reported when sphingomyelin was
consumed (Chung et al., 2013).

4.1.3 Butyric acid


Butyric acid (C4:0) found in milk fat is also linked to anticarcinogenic
activity (Bhat & Bhat, 2011). This four-carbon short-chain fatty acid is
present at a level of more than 3% in milk fat and butter (Stilling et al.,
2016; Verruck, Dantas, & Prudencio, 2019). Their presence is due to
microbial anaerobic fermentation of fiber in the ruminant gut (Stilling
et al., 2016). The anionic part of dissociated butyric acid and its salts, i.e.,
butyrate, mainly affects the gut and adjacent tissues beneficially (Canani
et al., 2011; Hamer et al., 2008). The consumption of butyrate is also linked
to other beneficial effects for health, such as energy homeostasis, obesity,
immune system regulation, cancer, and even brain function (Bourassa,
Alim, Bultman, & Ratan, 2016; Di Sabatino et al., 2005; Li, 2014;
Stilling et al., 2016). Research findings indicate that butyric acid may inhibit
the proliferation and induces apoptosis in a variety of cancer cell lines (colon,
leukemia, breast) (Aukema et al., 1997; Parodi, 1997a, 1997b; Smith &
German, 1995). Butyrate is also associated with down-regulation or inacti-
vation of the expression of cancer genes (Parodi, 1997a, 1997b; Smith &
German, 1995).

4.1.4 Myristic acid


Myristic acid, a long-chain saturated fatty acid (14:0), is one of the
most abundant fatty acids in milk fat (above 10%) (Verruck et al., 2019). This
fatty acid is known because it accumulates fat in the body, however, its
consumption also impacts positively on cardiovascular health. This behavior
is largely influenced by the balance between saturated fatty acid and simple
dietary carbohydrates in the diet (Ruiz-Núñez, Dijck-Brouwer, & Muskiet,
2016). Myristic acid is directly involved in post-translational protein changes
and mechanisms that control important metabolic processes in the human
body (Legrand & Rioux, 2015; Ruiz-Núñez et al., 2016). Dabadie,
Peuchant, Bernard, Leruyet, and Mendy (2005) reported that moderate
Dairy foods and positive impact on the consumer’s health 129

myristic acid consumption improves long-chain omega-3 fatty acids levels


in plasma phospholipids, which could exert improvement of cardiovascular
health parameters in humans. Another research by the same group
(Dabadie, Peuchant, Motta, Bernard, & Mendy, 2008) reported that the
consumption of myristic acid from dairy fat increased HDL cholesterol
and decreased triacylglycerides levels, while no changes in LDL cholesterol
were observed. Additional immunomodulatory functions are exerted by
myristic acid through the increase of a specific protein involved in activation
of macrophages in murine with high levels of myristic acid intake (Hubbard,
Socolich, & Erickson, 1996).

4.1.5 Vitamins
Butter also serves as an important carrier for fat-soluble vitamins (Parodi,
1997a, 1997b). Vitamin D is essential in maintaining calcium homeostasis
and skeleton integrity by promoting the intestinal absorption of calcium
and acting on bone mineralization (Christakos et al., 2016). According
to Pimpin et al. (2016), vitamin D consumption maintains the calcium
homeostasis, stimulates the insulin production and release, and regulates
the renin-angiotensin-aldosterone system to improve bone health. When
vitamin D synthesized by exposition to sunlight or consumed by food is
not in sufficient amount it results in rickets, soft and deformed bones. Butter
is one of the main foods that are a rich source of vitamin D (Mileševic et al.,
2018). Watkins et al. (1997) reported that the consumption of butter
lowered bone levels of arachidonic acid, which is a precursor of prosta-
glandin E2 (PGE2). PGE2 is a principal mediator of inflammation in diseases
such as rheumatoid arthritis and osteoarthritis (Park, Pillinger, & Abramson,
2006). The butter consumption also raised insulin-like growth factor
(IGF-1), moderated PGE2 production, and increased blood levels of
hexosamines and bone formation rate in young chicks (Watkins et al.,
1997). Therefore, high blood levels of vitamin E were also associated with
increased bone formation rate (Xu, Watkins, & Seifert, 1995). These authors
show that butter consumption may optimize vitamin E to enhance the
formation of bone due to an increase in the saturated/polyunsaturated fat
ratio in bone. Their findings indicate that butter consumption can optimize
bone formation by its effects on bone growth factors in chicks.

4.2 Nutritionally modified butter


Several modifications in milk fat can be made in order to improve the health
benefits of butter consumption. Because of the link between saturated fatty
130 Silvani Verruck et al.

acid consumption and increase in cholesterol, the reduction or removal of


cholesterol from milk fat is a continuous interest for the consumers
(Mortensen, 2011a, 2011b). Cholesterol reduction or removal can be done
through extraction, distillation, adsorption, enzymatic conversion, or
combinations thereof (Dias, Berbicz, Pedrochi, Baesso, & Matioli, 2010;
Kim, Jung, Ahn, & Kwak, 2006; Mohamed, Saldaña, Socantaype, &
Kieckbusch, 2000; Tahir & Lee, 2013). The extraction of cholesterol with
organic solvents in a single-stage or multiple-stage batch under vacuum can
be performed. However, since the use of organic solvents in food processing
is problematic, supercritical extraction with carbon dioxide can be a better
alternative (Mohamed et al., 2000).
Due to the different volatility of cholesterol and triacylglycerols found
in milk fat it can, therefore, be removed by vacuum steam distillation
and short-path molecular distillation efficiently. Nevertheless, the distilla-
tion process also removes the typical butter flavor, which is a problem
for the consumer (Mortensen, 2011a, 2011b). The complex cholesterol/
cyclodextrin can also be explored for cholesterol removal from milk fat
(Kim et al., 2006). This mechanism is based on the adsorption onto activated
carbon, diatomaceous earth, or specially coated glass, ceramics, or plastic
method (Dias et al., 2010; Kim et al., 2006; Tahir & Lee, 2013), and has
application in industrial scale (Mortensen, 2011b). The use of this process
has some advantages compared to the previous ones, such as simplicity,
low investment and less reduction in the volatile compounds of butter
(Dias et al., 2010; Tahir & Lee, 2013). Finally, the enzyme cholesterol reduc-
tase can also be used to remove cholesterol from milk fat. This enzyme
converts the cholesterol in compounds that cannot be absorbed and accumu-
lated in the human body; however, this process requires high production
costs (Mortensen, 2011b).
As reported previously, the CLA content can naturally be increased in
milk fat to produce enriched CLA-butter. The fatty acid content of milk
can be enhanced by increasing the monounsaturated or polyunsaturated
content of cows’ feed. This is achieved by feeding cows with full-fat soya
beans or a low-forage diet supplemented with oil, for example, sunflower
seed oil (Desroches et al., 2005; Haug et al. (2008); Penedo et al.,
2013; de Almeida et al., 2015). The modified diet results in an incomplete
biohydrogenation of PUFA in the rumen and greatly enhances the con-
centration of CLA in the milk (Mortensen, 2011b).
Another approach to improve beneficial effects of butter is the increase
in the long-chain polyunsaturated n–3 fatty acids content, i.e., omega-3
Dairy foods and positive impact on the consumer’s health 131

fatty acids. These fatty acids play an important role in blood pressure
maintenance, vision, brain development, cardiac functions, behavioral and
cognitive functions (Alessandri et al., 2004; Kris-Etherton, Grieger, &
Etherton, 2009; Kuratko, Cernkovich Barrett, Nelson, & Salem Jr., 2013;
Martinez-Micaelo et al., 2015). The most widely available source of
omega-3 fatty acids is salmon, herring, and mackerel, i.e., cold water oily fish
(Astorg, 2007). Populations that commonly have a traditional diet of marine
animals and fish, such as Eskimo people, Japan and Alaska, shows a lower
incidence of coronary diseases. Therefore, health authorities recommend a
certain intake of this fatty acid based on their health benefits (Mortensen,
2011b). As the omega-3 fatty acids content in milk is low, it depends on
the animal feed or direct addition of fish oil to the milk product (Lopez,
Blot, Briard-Bion, Cirie, & Graulet, 2017). Vanbergue et al. (2018) added
a new n-3 fatty acid source from microalgae and sieved extruded linseed
in cows’ corn silage-based diets. Milk obtained from cows fed with micro-
algae greatly increase the n-3 fatty acid content (0.444%) in comparison with
the control milk (0.019%). However, it was not possible to make butter from
this milk because no butter kernels were formed even after a long churning
time. The milk from sieved extruded linseed feed cows was able to make
butter with less yellow color, softer, with less rancid flavor and odor but
stronger cream flavor. In another study, butter was successfully supplemented
with nanoencapsulated beta-sitosterol, a phytosterol (Bagherpour, Alizadeh,
Ghanbarzadeh, Mohammadi, & Hamishehkar, 2017). Phytosterols are
known for their positive effects on reducing arteriosclerosis and cardio-
vascular diseases (Bagherpour et al., 2017). This study shows an interesting
opportunity for the dairy industry and promises great market potential.
Probiotic bacteria also can be added to butter in order to offer an
additional beneficial effect to consumers. These bacteria exert several
positive effects to the human health, such as lactose metabolization,
balancing of intestinal microbiota, enhanced immune system response and
anticarcinogenic properties (Ranadheera, Naumovski, & Ajlouni, 2018).
Lactobacillus maltaramicus and Lactobacillus casei subsp. casei decreased the
cholesterol content on a fat basis product (Aloglu & Oner, 2006). Although
milk fat has a protective effect on probiotic bacteria (Verruck et al., 2017),
few studies have investigated the effects of adding probiotics to butter.
Erkaya, Mustafa, Bayram, and B€ ulent (2015) added Bifidobacterium bifidum
ATCC 29521 and Lactobacillus acidophilus ATCC 4356 in butter and
evaluated their viability during 60 days of storage. According to their result,
25 g of butter per day provides a sufficient amount of probiotic bacteria to
132 Silvani Verruck et al.

exert the beneficial effects to health. Ewe and Loo (2016) produced butter
from Lactobacillus helveticus-fermented cream. In their work, the cream
fermentation with this bacteria modified nutritional and textural properties
of butter. The product had larger amounts of health beneficial unsaturated
fatty acids than the control and thus it led to a softer product. Olszewska,
Staniewski, and Łaniewska-Trokenheim (2012) evaluated during four-week
refrigerated storage the addition of Bifidobacterium lactis strain in butter and
concluded that butter should be considered also a source of probiotics. They
suggested that butter containing probiotic microorganisms might contribute
to the diversity on the probiotic markets, due to above minimal limit
of B. lactis presented in the studied butter. All these studies contribute to
an increased diversity of probiotic butter on the market.

5. Ice cream
Ice cream is one of the most known dairy products in all continents
and is a complex system, consisting of a frozen matrix containing air bubbles,
fat globules, ice crystals, and an unfrozen serum phase (Balthazar, Silva,
Cavalcanti, et al., 2017; Balthazar, Silva, Moraes, et al., 2017). Recently,
researchers have stated that ice cream, when consumed in moderation,
brings several health benefits. In fact, it can be considered a complete food
with high nutritional value, since it contains proteins, carbohydrates,
calcium, phosphorus, lipids, vitamins A, B1, B2, B6, C, D, E, and K, as well
as other minerals (Deosarkar, Kalyankar, Pawshe, & Khedkar, 2016;
Soukoulis & Tzia, 2018). Fig. 8 shows the role of ice cream consumption
on health.
The consumption of ice cream is also indicated in the diet of some
postoperative situations like withdrawal of tonsils and orthodontic surgeries
(Millington, Gaunt, & Phillips, 2016). It also is recommended for people
with gastroesophageal reflux and chemotherapy treatments (Bernish,
2019; Deosarkar et al., 2016). Willett, Stampfer, Colditz, Rosner, and
Speizer (1990), in a prospective study among women, studied the relation
of meat, fat, and fiber intake to the risk of colon cancer and reported that
ice cream was not significantly related to the risk of colon cancer. Recently,
a Brazilian researcher group developed an ice cream to be used in patients
who are undergoing chemotherapy. The ice cream favored salivation and
reduced the side effects caused by chemotherapy in the mouth, soothing
wounds, canker sores, mucositis, and dry mouth. However, the ice creams
developed for the study also acts as a food supplement. It is a high source of
Dairy foods and positive impact on the consumer’s health 133

Fig. 8 The role of ice cream consumption on health. Images: Freepik.

protein (isolated whey protein), fiber (polydextrose), low in fat content


(deodorized olive oil), and free of lactose (UFSC, 2018).
Another benefit of add isolated whey protein to ice cream is the increase
in their tryptophan content. This amino acid has a central role in the
serotonin production that modulate several brain functions, such as mood,
aggression, impulsivity, circadian rhythms and appetite (Silber & Schmitt,
2010). Some studies suggest that α-lactalbumin, which contains high
tryptophan values, when added to ice cream or other products lead to
improve brain serotonin activity, reduces cortisol concentration, improves
mood under stress, and also regulates the sleep time (Markus et al., 2005;
Markus et al., 2000; Minet-Ringuet, Le Ruyet, Tome, & Even,
2004). Grabenhorst, Rolls, Parris, and d’Souza (2010) measured the neural
activations of vanilla ice cream consumption through functional magnetic
resonance imaging and showed that ice cream has an immediate effect on
parts of the brain responsible for the sensation of pleasure and happiness.
These facts together could explain the good feeling that the consumers have
when consuming ice cream. Additionally, ice cream also is a rich source of
lactoferrin and cytokines, which improves the immunity against some
diseases like influenza (Deosarkar et al., 2016). It has also been demonstrated
in an in vivo study that the addition of lycopene to ice cream showed a
significantly better effect on patients’ acne (Chernyshova et al., 2019).
Calcium consumption is also recognized for its important role in
preventing osteoporosis and support bone formation. When the daily intake
134 Silvani Verruck et al.

of calcium is not sufficient, the body takes calcium from the bones and
teeth for essential functions (Deosarkar et al., 2016). Milk and dairy products
are widely recognized for its high calcium content in comparison with
other foods and, in addition, such calcium is better absorbed due to the
non-interference of antinutritional factors that are present in other foods
(Rozenberg et al., 2016). Van der Hee et al. (2009) developed an ice cream
formulation with calcium addition, lower in fat than regular ice cream,
which could provide a source of additional dietary calcium. Two ice cream
formulations were compared to milk calcium bioavailability in young adults.
Their results showed that the calcium absorption of the two ice cream
formulations were as high as for milk control, indicating that the ice cream
ingredients does not influence the delivery of calcium to the body. Ferrar
et al. (2011) designed a single-center randomized, double-blind, controlled
study with 80 premenopausal women (20–39 years) where calcium-fortified
ice cream was daily consumed for 28 days. The calcium-fortified ice cream
consumption reduced the levels of bone resorption marker while the body
weight did not change. Therefore, a serving of ice cream may be part of the
recommended daily intake of calcium (Ferrar et al., 2011). On the other
hand, the calcium intake is not good only for bones and teeth, but the
consumption of the indicated daily amount of calcium in the diet favors
the loss of weight. Fat cells grow larger when the body does not get the
proper amount of calcium. This lack of calcium leads to the increased
production of hormones that favor the production of body fat, which leads
to weight gain (Deosarkar et al., 2016).
After 8 years of testing, researchers found that among 18,555 women
who consumed more than two servings of ice cream per week had an
85% greater chance of not developing ovulation problems when compared
to women who consumed lower-fat dairy products. The conclusion was
that products with lower fat rates might interfere negatively in the fertility
of women, more specifically on a greater risk of anovulatory infertility
(Chavarro, Rich-Edwards, Rosner, & Willett, 2007). Wolford and
Argoudelsi (1979) reported that a higher estrogen concentration is present
in high-fat dairy products than in low-fat ones. This concentration can
explain the relation between ice cream consuming and fertility since the
insulin growth factor 1 protein levels are decreased by estrogens ( Jorgensen
et al., 2004; Veldhuis, Frystyk, Iranmanesh, & Orskov, 2005).
As ice creams are widely appreciated worldwide, regardless of culture,
age, and socioeconomic level, the supplementation of such foods with
prebiotic dietary oligosaccharides and or probiotic bacteria can add value
Dairy foods and positive impact on the consumer’s health 135

to the product by providing a functional appeal (Balthazar et al., 2018;


Balthazar, Silva, Cavalcanti, et al., 2017; Balthazar, Silva, Moraes, et al.,
2017). For functional ingredients denomination, probiotics are defined as
live microorganisms which when administered in adequate amounts, confer
a health benefit on the host (Hill et al., 2014). The probiotic effects are
strain-specific (Espitia, Batista, Azeredo, & Otoni, 2016) and they should
possess resistance to the gastric and bile acids, adhere to mucus or human
enteric epithelial cells, antimicrobial activity against pathogenic bacteria, bile
salt hydrolase activity, and ability to reduce pathogen adhesion to surfaces of
gastrointestinal tract (Kolacek et al., 2017). While prebiotics are “substrate
that is selectively utilized by host microorganisms conferring a health
benefit” (Gibson et al., 2017).
Ice creams are one of the most promising carriers for delivery of probiotic
bacteria to the intestine (Homayouni, Azizi, Javadi, Mahdipour, & Ejtahed,
2012). The high total solids, i.e., milk proteins, lactose, lipids, and other
contents in its composition, makes ice cream an ideal product for probiotic
delivery (Cruz, Antunes, Sousa, Faria, & Saad, 2009). The incorporation of
probiotic bacteria in ice cream can be made in both fermented and
unfermented mixes (Deosarkar et al., 2016). However, unfermented mixes
have a higher pH value, which can be an important advantage for probiotic
bacteria survival in ice cream (Akın & Ozt€ € urk, 2018). The most common
species of bacteria used as probiotics for its addition to ice cream are
Lactobacillus and Bifidobacterium (Cruz et al., 2009). The oxygen incorpora-
tion and freezing injury can represent factors that affect probiotic survival in
ice cream (Homayouni et al., 2012). Thus, a suitable approach must be used
to avoid freeze injury and oxygen toxicity, and this is directly related to
the ingredients used in the ice cream mix (Mohammadi, Mortazavian,
Khosrokhavar, & Da Cruz, 2011). Several studies incorporate probiotic
bacteria into ice creams with various formulations (Table 4), where many
of them have reported that ice cream is a good carrier of probiotics through-
out storage under freezing. When they are able to multiply, probiotic
bacteria produce substances like vitamin K, folic acid, biotin, thiamine,
riboflavin, cobalamin (B12), niacin, and pyridoxine that are beneficial for
human health (Akın & Ozt€ € urk, 2018). Furthermore, higher amounts of
B-group vitamins can be present in fermented probiotic ice cream in
comparison with unfermented probiotic ice cream (Gomes & Malcata,
1999). L(+)-lactic acid, which is more easily metabolized than D( )-lactic
acid, is also a relevant component produced by probiotic bacteria and used
as energy source by human metabolism (Gurr, 1987). Besides, the lactose
Table 4 Probiotic and/or prebiotic addition in ice cream.
Product Probiotic Prebiotic References
Ice cream Lactobacillus acidophilus and Lactobacillus rhamnosus – Abghari, Sheikh-Zeinoddin, and
Soleimanian-Zad (2011)
Peach ice Bifidobacterium lactis BB-12 Inulin Villalva et al. (2017)
cream
Ice cream Bifidobacterium lactis and Lactobacillus casei Camellia sinensis Noori, Khaji, and Gandoni (2017)
(prebiotic potential)
Ice cream Pediococcus pentosaceus UAM22 Inulin Fragoso et al. (2016)
Ice cream Lactobacillus paracasei subsp. paracasei, Bifidobacterium longum Polydextrose Açu, Kinik, and Yerlikaya (2017)
and Bifidobacterium bifidum
Goat milk Bifidobacterium animalis subsp. lactis BI-07 – Bezerra, Araujo, Santos, and Correia (2015)
frozen yogurt
Goat milk ice Bifidobacterium animalis subsp. lactis BI-07 – Silva, Bezerra, Santos, and Correia (2015)
cream
Low-fat ice Lactobacillus acidophilus La-5 and Bifidobacterium animalis Inulin and Akalın and Erişir (2008)
cream Bb-12 Oligofructose
Frozen Lactobacillus acidophilus LA-14 and Bifidobacterium lactis Inulin Akın, Akın, and Kırmacı (2007)
yogurt BL-01
Ice cream Lactobacillus rhamnosus GG – Alamprese, Foschino, Rossi, Pompei, and
Corti (2005)
Ice cream Lactobacillus johnsonii La1 – Alamprese, Foschino, Rossi, Pompei, and
Savani (2002)
Ice cream Lactobacillus acidophilus (ATCC 4357D-5) and – € urk, and Yilmaz (2018)
Ayar, Siçramaz, Ozt€
Bifidobacterium animalis subsp. lactis (ATCC 27536)
Table 4 Probiotic and/or prebiotic addition in ice cream.—cont’d
Product Probiotic Prebiotic References
Ice cream Lactobacillus acidophilus ATCC 4356 – Arslan et al. (2016)
Ice cream Lactobacillus acidophilus AB5–18, Lactobacillus agilis – Basyigit, Kuleaşan, and Karahan (2006)
AA17–73, Lactobacillus agilis AC18–88, Lactobacillus
rhamnosus AB20–100, Lactobacillus acidophilus AK4–14.
Butiá ice Bifidobacterium lactis (Bl-04) – Cruxen et al. (2017)
cream
Ice cream Bifidobacterium bifidum and Lactobacillus acidophilus – Christiansen, Edelsten, Kristiansen, and
Nielsen (1996)
Frozen Bifidobacterium longum and Lactobacillus acidophilus – Davidson, Duncan, Hackney, Eigel, and
yogurt Boling (2000)
Ice cream Lactobacillus rhamnosus DSM Inulin Di Criscio et al. (2010)
20,021 and Lactobacillus casei DSM 20011
Ice cream Lactobacillus plantarum, Lactobacillus casei, and Bifidobacterium Inulin, lactulose, and El-Sayed, Salama, and El-Sayed (2014)
bifidum oligofructose
Ice cream Bifidobacterium longum (BL-04) and Bifidobacterium lactis – Favaro-Trindade, Bernardi, Bodini, De
(BL-01) Carvalho Balieiro, and De Almeida (2006)
Ice cream Lactobacillus acidophilus 74–2, Lactobacillus acidophilus LAC 4 – Favaro-Trindade, De Carvalho Balieiro, Dias,
Amaral Sanino, and Boschini (2007)
Ice cream L. acidophilus DOWARU™ – Ferraz et al. (2012)
Ice cream Lactobacillus acidophilus 2401 and Bifidobacterium infantis – Godward and Kailasapathy (2003)
1912
Low-fat ice- Lactobacillus acidophilus Lafti" LI 10, Bifidobacterium lactis Resistant starch Hi Haynes and Playne (2002)
cream. BLC-h and Lactobacillus paracasei subsp. paracasei LCS-1 Maize™
Continued
Table 4 Probiotic and/or prebiotic addition in ice cream.—cont’d
Product Probiotic Prebiotic References
Ice cream Lactobacillus acidophilus and Bifidobacterium bifidum – Hekmat and McMahon (1992)
Ice cream Lactobacillus casei (Lc-01) and Bifidobacterium lactis (Bb-12) Resistant starch Hi Homayouni, Azizi, Ehsani, Yarmand, and
Maize™ Razavi (2008)
Ice cream Lactobacillus acidophilus, Lactobacillus casei, Bifidobacterium – Homayouni, Ehsani, Azizi, Razavi, and
bifidum, and Bifidobacterium longum Yarmand (2008)
Ice cream Lactobacillus acidophilus and Bifidobacterium lactis – Kailasapathy and Sultana (2003)
Ice cream Lactobacillus acidophilus (LA-5) and Lactobacillus casei – Karthikeyan, Elango, Kumaresan,
(NCDC-298) Golapakrishnamurty, and Raghunath (2014)
Ice cream Lactobacillus acidophilus la-5 and Bifidobacterium animalis – Magarinos, Selaive, Costa, Flores, and Pizarro
subsp. lactis BB-12 (2007)
Apple ice Lactobacillus acidophilus la-5 and Bifidobacterium animalis Inulin Matias, Padilha, Bedani, and Saad (2016)
cream subsp. lactis BB-12
Ice cream Lactobacillus acidophilus LMGP-21381 – Nousia, Androulakis, and Fletouris (2011)
Ice cream Lactobacillus casei 431 White and dark blue Ozt€€ urk, Demirci, and Akın (2017)
myrtle pulps (prebiotic
potential)
Ice cream Lactobacillus acidophilus NCDC 14 and Saccharomyces Fructooligosaccharide Pandiyan, Annal Villi, Kumaresan, Murugan,
boulardii and Gopalakrishnamurthy (2012)
Ice cream Lactobacillus acidophylus NCFM Yacon flour (prebiotic Parussolo et al. (2017)
potential)
Ice cream Lactobacillus acidophilus LA-5, Bifidobacterium animalis subsp. – Ranadheera, Evans, Adams, and Baines (2012,
lactis BB-12, and Propionibacterium jensenii 702 2013)
Ice cream Lactobacillus casei Shirota – Sagdic, Ozturk, Cankurt, and Tornuk (2012)
Table 4 Probiotic and/or prebiotic addition in ice cream.—cont’d
Product Probiotic Prebiotic References
Ice cream Lactobacillus gasseri B-14168, Lactobacillus rhamnosus B-445 – Salem, Fathi, and Awad (2005)
and Lactobacillus reuteri B-14171, Lactobacillus acidophilus
La-5 and Bifidobacterium bifidum BB-12
Fruit-based Lactobacillus acidophilus (LA 5) – Senanayake, Fernando, Bamunuarachchi, and
ice cream Arsekularatne (2013)
Ice cream Lactobacillus acidophilus (DSMZ 20079) and Bifidobacterium – Turgut & Cakmakci, 2009
bifidum (DSMZ 200456)
Strawberry Lactobacillus acidophilus Lyofast SLH 41107 – € uz (2007)
Vardar and Oks€
ice cream
Sheep milk – Inulin, Balthazar, Pimentel, Ferrão, et al. (2017) and
ice cream fructooligosaccharide, Balthazar, Silva, Moraes, et al. (2017)
galactooligosaccharide,
short-chain
fructooligosaccharide,
resistant starch, soluble
corn fiber, and
polydextrose
Sheep milk Lactobacillus casei-01 Inulin Balthazar et al. (2018)
ice cream
Açaı́ ice Lactobacillus rhamnosus GG – Costa, Ooki, Vieira, Bedani, and Saad (2017)
cream
Ice cream Lactobacillus casei – Gheisari, Ahadi, Khezli, and Dehnavi (2016)
fortified with
zinc
Frozen Bifidobacterium animalis subsp. lactis BB-12 Inulin Pinto et al. (2012)
yogurt
140 Silvani Verruck et al.

content in ice cream can be reduced through the use of probiotic bacteria,
once they metabolize lactose to consume glucose as an energy source
(Aboulfazli, Shori, & Baba, 2016).
An approach to support the survival of probiotic strains during
frozen storage may be based on the prebiotic addition on ice cream mix
(Akın & Ozt€€ urk, 2018). Table 4 shows studies where probiotic and/or
prebiotic were added to ice cream. The prebiotics are recognized for selec-
tively stimulating the development of probiotic bacteria, i.e., only these
bacteria use prebiotics as an energy source (Gibson et al., 2017). The viability
of Lactobacillus acidophilus La-5 and Bifidobacterium animalis Bb-12 improved
in ice cream when oligofructose was used in the formulation (Akalın &
Erişir, 2008). Some prebiotics may also exert dual function when added into
ice cream. In addition to serving as a substrate for probiotic bacteria, they are
known to be used to modify the texture of dairy products (Verruck et al.,
2019). Balthazar, Pimentel, Ferrão, et al. (2017), Balthazar, Silva,
Cavalcanti, et al. (2017), Balthazar, Silva, Moraes, et al. (2017) reported that
inulin is a promising alternative as fat substitutes in the formulation of sheep
milk ice cream due to rheological properties such as hardness, viscoelasticity,
and consistency similar to a product with fat. In addition, most prebiotic ice
creams have been reported to be sweeter than fat ice cream, suggesting that
these fibers may act as sweeteners (Balthazar, Pimentel, Ferrão, et al., 2017;
Balthazar, Silva, Cavalcanti, et al., 2017; Balthazar, Silva, Moraes, et al.,
2017). In ice cream, the addition of galactooligosaccharides presented a
positive effect on the physical-chemical, optical and sensorial characteristics.
In general, an increase in firmness and a decrease in melt rate was observed,
which contributes to greater product stability. From the sensorial point of
view, the ice cream supplemented with galactooligosaccharides stood out
by the taste and texture attributes (Balthazar et al., 2015). Soukoulis,
Lebesi, and Tzia (2009) reported that inulin could also be used as a controller
for crystallization and recrystallization phenomena in frozen dairy products.
Therefore, replacing milk fat with prebiotics for the manufacture of ice
cream may be an effective alternative to improve nutritional and physio-
logical aspects due to the low caloric value and functionality offered by
prebiotics (Akbari, Eskandari, Niakosari, & Bedeltavana, 2016).
Microencapsulation of probiotics can further protect these bacteria
from high sucrose concentrations, high oxygen, freezing, and storage temper-
atures in ice cream processing (Verruck, de Liz, Dias, Amboni, & Prudencio,
2018,Verruck, Santana, M€ uller, & Prudencio, 2018). Also, this process
can protect against acid (gastric conditions) and bile salts concentration
Dairy foods and positive impact on the consumer’s health 141

(intestinal conditions) (Verruck et al., 2017). The encapsulation provides


physical protection to probiotic and reduces cell loss by isolating the
bacterial cells from the adverse environment of the product and gastrointes-
tinal tract (Deosarkar et al., 2016). Add probiotic microcapsules in ice cream,
and frozen yogurts can provide better conditions for probiotic survival
for a long term of production, distribution, and storage (Cruz et al., 2009).
Thus, functional ingredients such as prebiotic or probiotic could
enhance health benefits in ice cream. For example, ice cream added with
prebiotics increase of overrun, color parameters; improve rheological
properties and sensory attributes; decrease ice crystals size and caloric value
(Balthazar, Silva, Cavalcanti, et al., 2017; Balthazar, Silva, Moraes, et al.,
2017). In addition, it could improve probiotic bacteria viability for a long
frozen shelf life (Balthazar et al., 2018). However, it is necessary to extend
this study to clinical trials, and thus a forthcoming study to evaluate the
survival of these microorganisms in the feces of healthy subjects consuming
the formulations assessed, since all of the ice cream matrices maintained the
minimum probiotic levels (Matias et al., 2016).

6. Dairy desserts
Dairy desserts comprise products with a diverse range of ingredients
and significant amounts of dairy ingredients (Saunders, 2011). These prod-
ucts include creamy and gelled desserts, custards/puddings, sachet desserts,
aerated desserts (mousses), cheesecakes and others (Saunders, 2011). This
product category has become increasingly popular with a significant volume
of ready-to-eat dairy desserts consumed globally (Verbeken, Bael, Thas, &
Dewetiinck, 2006). Convenience, nutrition, and sensory appeal are some of
the choices that lead to the popularity of these products. Traditionally dairy
desserts are not related to healthy foods; however, this dichotomy should be
reviewed (Horwath, Govan, & Campbell, 1995). The consumption of dairy
desserts may also be considered within the recommended daily portions of
dairy products for healthy diet maintenance (Ferrar et al., 2011). Saunders
(2011) reported that dairy desserts represent one of the better examples
of a healthy indulgence for consumers. This may be due to the protein,
fat, carbohydrates, calcium, phosphorus and some vitamins which may be
present in a serving of some dairy dessert (Ferrar et al., 2011). The high
nutritional value of the dairy ingredients used to make dairy desserts may
be one of the main factors involved in consumer choice.
142 Silvani Verruck et al.

Due to its soft texture and light flavor, some dairy desserts such as pud-
dings can be used in special health situations like dysphagia (Quinchia et al.,
2011). Dysphagia, which is a swallowing disorder, can affect people of all
ages and may be the result of neurological diseases, head, neck or tongue
cancer, or stroke (Logeman, 2007). The main goal of safe alimentation is
to prevent food from entering the airways, as this can lead to the development
of pneumonia. Aspiration depends on clinical status as well as liquid/food
flow properties, such as viscosity, consistency, adhesiveness, cohesion, and
volume of the swallowed food (Ozaki et al., 2010). Thus, if not well man-
aged, swallowing diseases can also lead to increased mortality due to weight
loss, dehydration, and malnutrition (Low, Wyles, Wilkinson, & Sainsbury,
2001). Because of these reasons, dairy desserts can be a good alternative
for these people, due to their quantity of nutrients, as well as their texture
of easy swallowing (Quinchia et al., 2011).
When the formulation of a dairy dessert is changed with the addition of
new ingredients, the functionality of the dessert also changes. This is the case
of D-psicose, a not caloric rare hexose that was added into raw materials of
custard pudding as a substitute for sucrose in order to develop a new func-
tional dessert (Sun, Hayakawa, Ogawa, & Izumori, 2007). The substitution
of sucrose by D-psicose increased the antioxidant activity of the pudding, so
this new product may be an alternative to be used by people who have dis-
eases caused by oxidative stress (Sun et al., 2007).
One of the main promising area on the modern dairy industry concerns
to the addition of probiotics and prebiotics in dairy desserts. This revolution-
izes the market, taking the dairy desserts to a functional food level. Table 5
shows studies in that probiotic and/or prebiotic were added to dairy desserts.
Among functional foods, probiotics, prebiotics and symbiotics are part of the
category of functional foods that assume other functions in the human body
beyond the basic function of nutrition (Granato, Branco, Cruz, de Faria, &
Shah, 2010). Around the world several health benefits have been attributed
to probiotic bacteria and numerous foods containing one or more groups of
probiotic organisms are available (Tripathi & Giri, 2014). Correct and reg-
ular administration can ensure the prevention of pathologies, regulation of
intestinal microbiota, disorders of gastrointestinal metabolism, immuno-
modulators and inhibition of carcinogenesis (Ranadheera et al., 2018).
The efficacy of probiotic bacteria added to dairy desserts also depends on
the level of the ingested population. To exert positive effects on health, these
microorganisms must be present in high numbers in the gastrointestinal
tract. The survival of probiotic culture over the shelf life of the product is
Dairy foods and positive impact on the consumer’s health 143

Table 5 Probiotic and/or prebiotic addition in dairy desserts.


Product Probiotic Prebiotic References
Pudding Lactobacillus casei – Gul (2017)
Shirota
Cacao Lactobacillus acidophilus – Irkin & Guldas, 2011
pudding LAFTIs L10 and
Bifidobacterium animalis
ssp. lactis LAFTI B94
and Lactobacillus casei
LAFTI L26
Chocolate Lactobacillus rhamnosus Glucan type İspirli, Demirbaş, and
pudding GG exopolysaccharide Dertli (2018)
Chocolate Lactobacillus paracasei Inulin Aragon-Alegro,
mousse subsp. paracasei LBC 82 Alarcon Alegro,
Roberta Cardarelli,
Chih Chiu, and Isay
Saad (2007)
Chocolate Lactobacillus paracasei Fructooligosaccharide Valencia et al. (2016)
mousse subsp. paracasei LBC 81 P95
Chocolate Lactobacillus paracasei Inulin Patel, Parekh, and
mousse subsp. paracasei NCDC Subhash (2008)
022
Chocolate Lactobacillus paracasei Inulin Cardarelli, Aragon-
mousse subsp. paracasei LBC 82 Alegro, Alegro,
de Castro, and
Saad (2008)
Chocolate Lactobacillus acidophilus – Rosa et al. (2015)
dessert La-5
Chocolate Lactobacillus casei Lpc – Silva et al. (2013)
flan 37
Passion Lactobacillus acidophilus Inulin Buriti, Komatsu, and
fruit and La–5 Saad (2007)
guava
mousses
Guava Lactobacillus acidophilus Inulin Buriti, Castro, and
mousse La-5 Saad (2010)
Guava Lactobacillus acidophilus Inulin and Komatsu et al. (2013)
mousse La-5 oligofructose P95
Continued
144 Silvani Verruck et al.

Table 5 Probiotic and/or prebiotic addition in dairy desserts.—cont’d


Product Probiotic Prebiotic References
Coconut Bifidobacterium lactis – Corr^ea, Castro, and
flan BL-04 and Lactobacillus Saad (2008)
paracasei subsp.
paracasei LBC 82
Rice Lactobacillus acidophilus – Ozcan, Yilmaz-Ersan,
pudding LA-5 and Akpinar-Bayizit,
Bifidobacterium bifidum Irmak Sahin, and
BB-12 Aydinol (2010)
Cereal Lactobacillus acidophilus Polydextrose Helland, Wicklund,
pudding La5 and 1748, Litesse™ and Narvhus (2004)
Bifidobacterium animalis
Bb12, and Lactobacillus
rhamnosus GG
Fermented Lactobacillus acidophilus – Shah and Ravula
dessert MJLA1 and (2000)
Bifidobacterium spp.
BDBB2
Fermented Mixed culture of – Tavares Estevam et al.
dessert Bifidobacterium animalis (2017)
subsp. lactis and
Lactobacillus acidophilus
(SAB 440-A)

critical in all types of probiotic dairy desserts. A daily dose of 108–1010 CFU
probiotic bacteria is required for health benefits, which represents the con-
sumption of 100 g of the food, containing at least 106 CFU/g (Boylston,
Vinderola, Ghoddusi, & Reinheimer, 2004). The interactions between
probiotic bacteria and ingredients used in the formulation, the manufacturing
method and dairy dessert storage should be carefully evaluated in order to
not interfere with the survival of probiotic bacteria (Champagne, Gomes
da Cruz, & Daga, 2018; Tripathi & Giri, 2014).
Several prebiotic ingredients can be used in dairy desserts, e.g.,
inulin, fructooligosaccharides, lactulose, lacto-sucrose, lactitol, galactooligo-
saccharide, soy oligosaccharides, isomaltooligosaccharide, xylooligosaccharide,
honey oligosaccharides, the gentio-oligosaccharide and/or combinations
thereof (Aragon-Alegro et al., 2007; Buriti, Bedani, & Saad, 2016; Cardarelli
et al., 2008; Patel et al., 2008; Valencia et al., 2016). Moreover, these desserts
can be made from milk of different animals (e.g., bovine, goat, sheep, buffalo,
Dairy foods and positive impact on the consumer’s health 145

camel) and milks that have different fat content (skimmed, partially skimmed,
whole) (Gopal, Kalla, Manthani, & Keerthi, 2017). Frozen dairy desserts in
particular have potential for the development of low-fat products and conse-
quently may result in an increase in sales of this segment on the market
(Olson, White, & Watson, 2003). Also, due to a great consumer acceptance,
chocolate dairy desserts may represent new alternatives for symbiotic products
(Valencia et al., 2016). In addition to the health benefits attributed to the
consumption of products containing prebiotics, the addition of inulin has been
related to the improvement in the structure and texture of food products, since
it is able to act as a substitute for fat, besides exerting a cryoprotective effect for
probiotic in dairy desserts (Krasaekoopt & Bhandari, 2012).

7. Conclusions
Milk is considered as a healthy product with substantial health benefits.
Therefore, dairy foods, such as fermented milk, cheese, butter, ice cream,
and dairy dessert could be considered an essential component of an
equilibrated diet from a nutritional and functional point of view. It is note-
worthy that they are excellent sources of proteins and minerals, especially
calcium in a highly bioavailable form. Dairy products can also be considered
an excellent matrix for the release of bioactive compounds. Also, GABA and
CLA are important metabolites released by LAB and present in the milk fat,
have shown potential in disease prevention. Other important compounds
such as exopolysaccharides, which enhance the rheological properties of
yogurts, can have antioxidant, antimicrobial, and immunological properties.
Dairy products can improve health or well-being and, when consumed at
recommended levels, their benefits include improved immune system
function, reduced risk of cardiovascular, reduced risk of bone mass loss,
and protection against free radical damage. When dairy products are added
with probiotic, prebiotic and/or symbiotic, they can prevent gastrointestinal
diseases. Finally, a better understanding of components responsible for the
nutritional and functional value of dairy products, and their underlying mech-
anism were crucial to elucidate the positive impact on consumer’s health.

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Further reading
Belury, M. A., Moya-Camarena, S. Y., Lu, M., Shi, L., Leesnitzer, L. M., & Blanchard, S. G.
(2002). Conjugated linoleic acid is an activator and ligand for peroxisome proliferator-
activated receptor-gamma (PPAR). Nutrition Research, 22, 817–824.
Pimentel, T. C., Aparecida Marcolino, V., Eduardo Barão, C., Jensen Klososki, S., &
Rosset, M. (2017). Minas Frescal cheese as a probiotic carrier. In J. M. Merillon &
K. G. Ramawat (Eds.), Bioactive molecules in food (pp. 1–32): Springer International
Publishing.

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