ArticlePDF AvailableLiterature Review

Yogurt and gut function

Authors:

Abstract

In recent years, numerous studies have been published on the health effects of yogurt and the bacterial cultures used in the production of yogurt. In the United States, these lactic acid-producing bacteria (LAB) include Lactobacillus and Streptococcus species. The benefits of yogurt and LAB on gastrointestinal health have been investigated in animal models and, occasionally, in human subjects. Some studies using yogurt, individual LAB species, or both showed promising health benefits for certain gastrointestinal conditions, including lactose intolerance, constipation, diarrheal diseases, colon cancer, inflammatory bowel disease, Helicobacter pylori infection, and allergies. Patients with any of these conditions could possibly benefit from the consumption of yogurt. The benefits of yogurt consumption to gastrointestinal function are most likely due to effects mediated through the gut microflora, bowel transit, and enhancement of gastrointestinal innate and adaptive immune responses. Although substantial evidence currently exists to support a beneficial effect of yogurt consumption on gastrointestinal health, there is inconsistency in reported results, which may be due to differences in the strains of LAB used, in routes of administration, or in investigational procedures or to the lack of objective definition of "gut health." Further well-designed, controlled human studies of adequate duration are needed to confirm or extend these findings.
Review Article
Yogurt and gut function
1, 2
Oskar Adolfsson, Simin Nikbin Meydani, and Robert M Russell
ABSTRACT
In recent years, numerousstudies have been published onthe health
effects of yogurt and the bacterial cultures used in the production of
yogurt. In the United States, these lactic acid–producing bacteria
(LAB) include Lactobacillus and Streptococcus species. The bene-
fits of yogurt and LAB on gastrointestinal health have been inves-
tigatedinanimalmodelsand,occasionally,inhumansubjects.Some
studiesusing yogurt, individualLAB species, orboth showedprom-
ising health benefits for certain gastrointestinal conditions, includ-
ing lactose intolerance, constipation, diarrheal diseases, colon can-
cer, inflammatory bowel disease, Helicobacter pylori infection, and
allergies.Patientswithanyoftheseconditionscouldpossiblybenefit
fromtheconsumptionofyogurt.Thebenefitsofyogurtconsumption
to gastrointestinal function are most likely due to effects mediated
through the gut microflora, bowel transit, and enhancement of gas-
trointestinal innate and adaptive immune responses. Although sub-
stantial evidence currently exists to support a beneficial effect of
yogurtconsumptionongastrointestinalhealth,thereisinconsistency
in reported results, which may be due to differences in the strains of
LAB used, in routes of administration, or in investigational proce-
dures or to the lack of objective definition of “gut health.” Further
well-designed, controlled human studies of adequate duration are
needed to confirm or extend these findings. Am J Clin Nutr
2004;80:245–56.
KEY WORDS Yogurt, gut function, gut immunity, gastroin-
testinal diseases, gut microflora
INTRODUCTION
Components of the human intestinal microflora and of the
foodenteringtheintestinemayhaveharmfulorbeneficialeffects
on human health. Abundant evidence implies that specific bac-
terial species used for the fermentation of dairy products such as
yogurt and selected from the healthy gut microflora have pow-
erfulantipathogenic and antiinflammatory properties. These mi-
croorganismsare therefore involved with enhanced resistance to
colonizationofpathogenicbacteriaintheintestine,whichhasled
to the introduction of novel modes of therapeutic and prophy-
lactic interventions based on the consumption of monocultures
and mixed cultures of beneficial live microorganisms as “probi-
otics.” Probiotics are defined as “living microorganisms, which
on ingestion in sufficient numbers, exert health benefits beyond
inherent basic nutrition” (1).
Yogurt is one of the best-known of the foods that contain
probiotics. Yogurt is defined by the Codex Alimentarius of 1992
asacoagulatedmilkproductthatresultsfromthefermentationof
lactic acid in milk by Lactobacillus bulgaricus and Streptococ-
cus thermophilus (2). Other lactic acid bacteria (LAB) species
are now frequently used to give the final product unique charac-
teristics. As starter cultures for yogurt production, LAB species
display symbiotic relations during their growth in milk medium
(3). Thus, a carefully selected mixtureof LAB species is usedto
complementeachotherandtoachievearemarkableefficiencyin
acid production. Furthermore, to increase the number of LAB
that survive the low pH and high acidity of the gastrointestinal
environment, some LAB species that are indigenous to the hu-
man intestine have been used in yogurt production. To meet the
National Yogurt Association’s criteria for “live and active cul-
ture yogurt,” the finished yogurt product must contain live LAB
inamounts 10
8
organisms/gatthetimeofmanufacture(3),and
the cultures must remain active at the end of the stated shelf life,
as ascertained with the use of a specific activity test.
In many modern societies, fermented dairy products make up
a substantial proportion of the total daily food consumption.
Furthermore, it has long been believed that consuming yogurt
and other fermented milk products provides various health ben-
efits(4). Studies fromthe1990son the possiblehealthproperties
of yogurt added to this belief (1, 5).
Probiotic therapy is based on the notion that there is such a
thing as a “normal” healthy microflora, but normal healthy mi-
croflora has not been defined except perhaps as microflora with-
out a pathogenic bacterial overgrowth. The development of
novel means of characterizing and modifying the gut microflora
has opened up new perspectives on the role of the gut microflora
in health and disease. Numerous studies suggested beneficial
therapeutic effects of LAB on gut health. However, results have
been inconsistent, which may be due to differences in the strains
ofLAB, routesofadministration, andinvestigationalprocedures
used in these studies.
Several LAB species are currently used in the production of
yogurt. This review focuses on the current evidence suggesting
that yogurt and specific LAB species that are used for the fer-
mentation of milk may or may not have valuable health-
promoting properties or therapeutic effects on various gastroin-
testinal functions and diseases.
1
FromtheJeanMayerUSDAHumanNutritionResearchCenteronAging
at Tufts University, Boston.
2
Address reprint requests to SN Meydani, Nutritional Immunology Lab-
oratory, JM USDA-HNRCA at Tufts University, 711 Washington Street,
Boston, MA 02111. E-mail: simin.meydani@tufts.edu.
Received October 3, 2003.
Accepted for publication February 12, 2004.
245Am J Clin Nutr 2004;80:245–56. Printed in USA. © 2004 American Society for Clinical Nutrition
by guest on June 6, 2011www.ajcn.orgDownloaded from
NUTRITIONAL VALUE OF YOGURT
The nutrient composition of yogurt is based on the nutrient
composition of the milk from which it is derived, which is af-
fected by many factors, such as genetic and individual mamma-
lian differences, feed, stage of lactation, age, and environmental
factors such asthe season of the year.Other variables that play a
role during processing of milk, including temperature, duration
of heat exposure, exposure to light, and storage conditions, also
affect the nutritional value of the final product. In addition, the
changes in milk constituents that occur during lactic acid fer-
mentation influence the nutritional and physiologic value of the
finished yogurt product. The final nutritional composition of
yogurt is also affected by the species and strains of bacteria used
in the fermentation, the source and type of milk solids that may
be added before fermentation, and the temperature and duration
of the fermentation process.
B vitamins
Dairy products have generally been considered an excellent
source of high-quality protein, calcium, potassium, phosphorus,
magnesium, zinc, and the B vitamins riboflavin, niacin, vitamin
B-6, and vitamin B-12 (6). A much greater loss of vitamins than
of minerals may occur during the processing of yogurt because
vitamins are more sensitive to changes in environmental factors
than are minerals. Some of the factors that are important during
theprocessing ofmilkand thatareknownto haveadverseeffects
on the vitamin content of dairy products in general include heat
treatment and pasteurization, ultrafiltration, agitation, and oxi-
dative conditions. In addition, bacterial cultures used during the
fermentationprocessof yogurt can influence the vitamin content
of the final product (6).
LAB species do require B vitamins for growth, but some
cultures are capable of synthesizing B vitamins (6). An example
of a B vitamin that is utilized by LAB is vitamin B-12 (7, 8).
Vitamins required for the growth of LAB cultures vary from one
strain to another. Significant losses of vitamin B-12 can be cor-
rected by the careful use of supplementary LAB cultures that are
capable of synthesizing vitamin B-12 (9).
Folate is the best example of a B vitamin that some LAB
species synthesize (10, 11). Depending on the bacterial strains
used, the folate content of yogurt can vary widely, ranging from
4to19
g/100 g (8). The major form of folate present in milk is
5-methyl-tetrahydrofolate (12). In a recent study, bacterial iso-
lates from various species used for milk fermentation and yogurt
productionwereexaminedfortheirabilitytosynthesizeorutilize
folate (11). S. thermophilus and Bifidobacteria were folate pro-
ducers, whereas Lactobacilli depleted folate from the milk me-
dia. A combination of folate-producing cultures resulted in even
greater folate content of the final fermented product. Further
studies on the effect of changes in the vitamin B content of milk
on fermentation would be of great practical significance.
Lactose
Dairy productsand foodsprepared with the use of dairy ingredi-
ents are an exclusive source of the disaccharide lactose in human
diets. Before absorption, lactose is hydrolyzed by the intestinal
brush border
-galactosidase (lactase) into glucose and galactose.
These monosaccharides are absorbed and used as energy sources.
Before fermentation, the lactose content of the yogurt mix gen-
erally is 6% (3). One example of a significant bacteria-induced
changethat occursduringthefermentationprocess isthehydrolysis
of 2030% of the disaccharide lactose to its absorbable monosac-
charide components, glucose and galactose (2). In addition, a por-
tion of the glucose is converted to lactic acid. Depending on other
ingredients added, this hydrolysis results in lower lactose concen-
trations in yogurtthan inmilk, which inpart explainswhy yogurt is
toleratedbetter thanmilkbypersonswith lactosemaldigestion(13
15). However, other factors also seem to play a role. For example,
lactose-intolerantsubjectsexhibitedbettertoleranceforyogurtwith
arelativelyhighamountoflactosethanformilkcontainingasimilar
amount of lactose (13, 15). In another example, bacteria present in
yogurt, such as L. bulgaricus and S. thermophilus, expressed func-
tional lactase, the enzyme that breaks down lactose (16). This ex-
pression may also contribute tobetter tolerance of lactose inyogurt
than of lactose in milk by persons with lactose maldigestion (15).
Protein
The protein content of commercial yogurt is generally higher
thanthatofmilkbecauseoftheadditionofnonfatdrymilkduring
processing and concentration, which increases the protein con-
tent of the final product. It has been argued that protein from
yogurt is more easily digested than is protein from milk, as
bacterial predigestion of milk proteins in yogurt may occur (8,
17). This argument is supported by evidence of a higher content
offreeaminoacids,especiallyprolineandglycine,inyogurtthan
in milk. The activity of proteolytic enzymes and peptidases is
preserved throughout the shelf life of the yogurt. Thus, the con-
centration of free amino groups increases up to twofold during
the first 24 h and then doubles again during the next 21 d of
storage at 7 °C (18). Some bacterial cultures have been shown to
have more proteolytic activity than do others. For example, L.
bulgaricuswasshown to have a much higher proteolytic activity
during milk fermentation and storage than does S. thermophilus,
as indicated by elevated concentrations of peptides and free
amino acids after milk fermentation (19).
During fermentation, bothheat treatment and acid production
resultinfinercoagulationofcasein,whichmayalsocontributeto
thegreaterproteindigestibilityofyogurtthanofmilk.Proteinsin
yogurt are of excellent biological quality, as are those in milk,
because the nutritional value of milk proteins is well preserved
during the fermentation process (20). Both the caseins and the
wheyproteinsinyogurtarerichsourcesofalltheessentialamino
acids,andtheintestinalavailabilityofnitrogenhasbeenreported
as being high (93%; 21, 22). Labeling of milk proteins with the
stable isotope
15
N has made it possible to discriminate between
exogenous and endogenous nitrogen fractions in serum after
ingestion of
15
N-labeled milk or
15
N-labeled yogurt proteins. In
a study of human subjects, Gaudichon et al (23) found that pro-
teins from both milk and yogurt were rapidly hydrolyzed after
ingestion,butthegastroduodenaltransferofdietarynitrogenwas
slower when yogurt was fed than when milk was fed.
Lipids
Milk fat also goes through biochemical changes during the
fermentation process. Minor amounts of free fatty acids are re-
leasedasaresultoflipaseactivity(3).Becausemostoftheyogurt
sold in the United States is of the low-fat and nonfat varieties,
hydrolysis of lipids contributes little to the attributes of most
yogurt products. However, yogurt hasbeen shown to have a higher
concentration of conjugated linoleic acid (CLA), a long-chain
246 ADOLFSSON ET AL
by guest on June 6, 2011www.ajcn.orgDownloaded from
biohydrogenatedderivativeoflinoleicacid,thandoesthemilkfrom
which the yogurt was processed (24). A fermented dairy product
from India, referred to as dahi, has also been shown to have higher
CLA content thandoes nonfermented dahi(25). Themajor sources
of CLA in our diets are animal products from ruminants, in which
CLA is synthesized by rumen bacteria. Increased consumption of
dairy fat was shown to be associated with increased concentrations
of CLA in both human adipose tissue (26) and human milk (27). It
washypothesizedthatbiohydrogenationalsooccursduringfermen-
tationofmilkandresultsinhigherconcentrationsofCLAinthefinal
product (28).
CLA was reported to have immunostimulatory and anticarci-
nogenic properties (29). In a recent study of breast and colon
cancer cells, Kemp et al (30) showed that the anticarcinogenic
propertiesofCLAmaybeduetotheabilityofsomeCLAisomers
to inhibit the expression of cyclins and thus halt the progression
ofthecellcyclefromG1toSphase.Inaddition,CLAinducedthe
expression of the tumor suppressor p53.
Minerals
In addition to being a good source of protein, yogurt is an
excellent source of calcium and phosphorus. In fact, dairy prod-
ucts such as milk, yogurt, and cheese provide most of the highly
bioavailable calcium in the typical Western diet. Because of the
lower pH of yogurt compared with that of milk, calcium and
magnesium are present in yogurt mostly in their ionic forms.
Oneof the major functionsofcalciumis the role itplaysinbone
formation and mineralization. The calcium requirements during
growth, pregnancy, andlactation are increased. However, theaver-
age calcium intake of women of childbearing age is consistently
less than is recommended (31). In addition, calcium intake of
womentendsto fall even lower during thepostmenopausalyears
(32). This is especially important for postmenopausal women,
who are at increased risk of bone loss and osteoporosis. Dietary
fiber has an adverse effect on calcium absorption, whereas lac-
tose may enhance the absorption of calcium (33). In the rat
model, calcium retention was greater with consumption of a diet
in which lactose made up half the total carbohydrates ingested
than with consumption of the control diet (34). Schaafsma et al
(35), investigating the effect of dairy products on mineral ab-
sorption by using rat models, reported that lactose enhances the
absorptionofcalcium,magnesium, andzinc.Becauseyogurthas
a lactose content lower than that of milk, the bioavailability of
these minerals maybe negatively affected, although the effect is
likely to be small.
The acidic pH of yogurt ionizes calcium and thus facilitates
intestinal calcium uptake (36). The low pH of yogurt also may
reduce the inhibitory effect of dietary phytic acid on calcium
bioavailability. Vitamin D plays a major regulatory role in in-
testinal calcium absorption. The active, saturable, transcellular
route of calcium absorption in the duodenum and proximal jeju-
num requires calbindin-D, a vitamin Ddependent calcium-
binding protein (37). In the United States, milk and infant for-
mula are fortified with vitamin D, and hence they serve as good
dietarysources,with2.5
g(100IU)vitaminD/237-mLserving.
However, other dairy products, such as yogurt, typically are not
fortified with vitamin D.
Few studies have investigated the effect of yogurt-derived
calcium on bone mineralization in animals (34, 38). Kaup et al
(34) reported that yogurt-fed rats showed greater bone mineral-
ization than did rats fed a diet containing calcium carbonate.
These studies may suggest that the bioavailability of calcium in
yogurt is greater and yogurt may increase bone mineralization
more than do nonfermented milk products. However, there are
currently no published studies that show a superior effect of
yogurt on bone mineralization in human subjects.
MECHANISTIC RATIONALE FOR POTENTIAL
BENEFITS OF YOGURT ON GUT FUNCTION AND
HEALTH
It has been suggested that yogurt and LAB contribute to sev-
eral facets of gastrointestinal health: the makeup of the gastro-
intestinal flora, the immune response, and laxation.
Gut microflora
Lactobacilli are among the components of microbial flora in
both the small and large intestines. The ability of nonpathogenic
intestinal microflora, such as LAB, to associate with and bindto
the intestinal brush border tissue is thought to be an important
attribute that prevents harmful pathogens from accessing the
gastrointestinal mucosa (39). For LAB to have an effect, they
must adapt to the host intestinal environment and be capable of
prolonged survival in the intestinal tract (4043). LAB survival
is influenced by gastric pH as well as by exposure to digestive
enzymes and bile salts (42), and LAB species differ in their
ability to survive in the gastrointestinal environment (43).
When 4 strains of Bifidobacterium (B. infantis, B. bifidum, B.
adolescentis,andB. longum) were compared, B. longum was the
most resistant to the effects of gastric acid (44). Bifidobacterium
animalis was reported to have a high survival rate during intes-
tinal transit in human subjects (45).
The effect of feeding yogurt fermented with S. thermophilus,
L. bulgaricus, and Lactobacillus casei on the fecal microflora of
healthy infants aged 1018 mo was investigated by Guerin-
Danan et al (46). Whereas the number of infants with fecal
Lactobacillus increased after the feeding, the total numbers of
anaerobes, Bifidobacteria, bacteroides, and enterobacteria were
not affected by yogurt intake. In a group of elderly patients with
atrophic gastritis and hypochlorhydria, Lactobacillus gasseri
survived passage through the gastrointestinal tract, but S. ther-
mophilus and L. bulgaricus were not recovered (43). Bifidobac-
terium sp has also been shown to survive passage through the
gastrointestinal tract: fecal concentrations were detectable for
8 d after the cessation of intake (47).
Anotherimportantfactorthatlimitsthesurvival oflactobacilli
withintheuppergastrointestinaltractistheinherentabilityofthe
organisms to adhere to intestinal epithelial cells (42). With the
use of scanning electron microscopy, Plant and Conway (48)
screened 16 strains of Lactobacillus for their capacity to associ-
ate with Peyers patches and the lymphoid villous intestinal tis-
sues in mice. Two of the 16 strains investigated, Lactobacillus
acidophilus and L. bulgaricus, are of interest because they relate
to yogurt. Itwas found, in both in vitro and in vivo models using
BALB/c mice, that L. bulgaricus did not associate with Peyers
patches or with the lymphoid villous intestinal tissues. L. aci-
dophilus had a low degree of association with Peyers patches
andno association to the lymphoid villous intestinal tissue. Nev-
ertheless, the authors stated that the strains of Lactobacillus
tested showed high rates of survival when Lactobacillus was
administered orally.
YOGURT AND GUT FUNCTION 247
by guest on June 6, 2011www.ajcn.orgDownloaded from
Theabilityof LAB to decrease the gastrointestinalinvasionof
pathogenicbacteriahasalsobeen described (39, 49). Bernet et al
(39) reported a dose-dependent L. acidophilusmediated inhibi-
tion of the adherence of enteropathogenic Escherichia coli and
Salmonella typhimurium to the enterocyte cell-line Caco-2. In
addition, L. acidophilus inhibited the entry of E. coli, S. typhi-
murium, and Yersinia pseudotuberculosis into Caco-2 cells. In
anotherreport(49),thesameauthorsdescribedsimilarinhibitory
effectswhen2differentstrainsofBifidobacteria(B.breveandB.
infantis)wereused.Inaddition,long-termfeedingofyogurtdoes
notresultinasignificantchangeintheresultsofbreath-hydrogen
tests, which indicates the absence of a significant change in the
intestinal survival of the yogurt organisms (50). Furthermore, it
is possible that the ability of LAB to compete with pathogens for
adhesion to the intestinal wall is influenced by their membrane
fluidity.This possibility wassuggestedbystudies indicating that
the type and quantities of polyunsaturated fatty acids in the ex-
tracellularmilieuinfluencetheadhesivepropertiesofLABtothe
epithelium (51, 52).
Gut-associated immune response
Themucosallymphoidtissueofthegastrointestinaltractplays
animportantrole as a firstlineofdefenseagainst ingested patho-
gens. The interactions of LAB with the mucosal epithelial lining
of the gastrointestinal tract, as well as with the lymphoid cells
residing in the gut, have been suggested as the most important
mechanism by which LAB enhances gut immune function. Sev-
eral factors have been identified as contributing to the immuno-
modulating and antimicrobial activities of LAB, including the
production of low pH, organic acids, carbon dioxide, hydrogen
peroxide, bacteriocins, ethanol, and diacetyl; the depletion of
nutrients; and competition for available living space (1, 5, 53).
The gastrointestinal tract is a complex immune system tissue.
Themainsiteofthemucosalimmunesysteminthegutisreferred
to as gut-associated lymphoid tissue (GALT), which can be di-
vided into inductive and effector sites. In the small intestine, the
inductive sites are in the Peyers patches, which consist of large
lymphoid follicles in the terminal small intestine. The best-
defined effector component of the mucosal adaptive immune
system is secretory immunoglobulin A (sIgA). sIgA is the main
immunoglobulin of the humoral immune response, which to-
gether with the innate mucosal defenses provides protection
against microbial antigens at the intestinal mucosal surface (54).
In a healthy person, sIgA inhibits the colonization of pathogenic
bacteria in the gut, as well as the mucosal penetration of patho-
genic antigens. At least 80% of all the bodys plasma cells, the
source of sIgA, are located in the intestinal lamina propria
throughout the length of the small intestine. IgA is the most
abundantly produced immunoglobulin in the human body. The
productionofintestinalsIgArequiresthepresenceofcommensal
microflora (55), which indicates that the production of intestinal
sIgA is induced in response to antigenic stimulation. It is not yet
clear, however, how lamina propria B cells are activated to be-
comeIgA-secretingplasmacellsorhowthe intestinalmicroflora
influence this process. Most studies on the effect of fermented
milk or specific LAB on gut immune function have centered on
their immune adjuvant effects in the gut.
The ability of LAB to modulate IgA concentrations in the gut
has also been the subject of several studies. Orally administered
L. acidophilus and L. casei and the feeding of yogurt increased
both IgA production and the number of cells secreting IgA in the
small intestine of mice in a dose-dependent manner (5). Simi-
larly, a report by Puri et al (56) indicated that S. typhimurium-
induced serum IgA concentrations were significantly higher in
mice fed yogurt over a period of 4 wk than in milk-fed control
mice.ThisreportsuggeststhattheIgAsecretedbythechallenged
intestinal B cells enters the circulation and increases the concen-
trations of IgA in the serum. Thus the IgA-enhancing effect of
yogurt intake may have both an effect on the gut and a systemic
effect. The same study also showed that intestinal lymphocytes
frommice fedyogurthad ahighermitogen-induced proliferative
response after a challenge with S. typhimurium than did those
from control-fed mice.
In a study using human subjects, Link-Amster et al (57)
showed that the specific anti-IgA titer to S. typhimurium was 4
times greater in subjects fed fermented milk containing L. aci-
dophilus than in control subjects fed diets without fermented
milk. Total sIgA concentrations also increased in subjects fed
fermented milk.
Macrophages play an important role as a part of the innate
immune response in the gut, and they represent one of the first
lines of nonspecific defense against bacterial invasion. The ef-
fects of feeding milk fermented with either L. casei or L. aci-
dophilus or both on the specific and nonspecific host defense
mechanisms in Swiss mice were investigated by Perdigon et al
(58). They showed that feeding milk fermented with L. casei, L.
acidophilus, or both for 8 d increased the in vitro and in vivo
phagocytic activity of peritoneal macrophages and the produc-
tion of antibodies to sheep red blood cells. The activation of the
immune system beganon day 3, peaked on day 5, anddecreased
somewhat on day 8 of feeding. Phagocytic activity was further
boosted in mice given a single dose of fermented milk on day 11
of feeding.
Modulation of cytokine production by yogurt and LAB has
also been the focus of several studies. In addition to interleukin
(IL)-1
and tumor necrosis factor (TNF)
, which are mainly
producedbymacrophages,T lymphocytesarethesourceof most
cytokines investigated in those reports. T cells are frequently
classifiedinto2categoriestype1(Th1)andtype2(Th2)helper
T cells. On activation, these cells produce 2 diverse patterns of
cytokines (59). Th1 cells are the main producers of interferon-
(IFN-
) and IL-2, and Th2 cells produce IL-4, IL-5, IL-6, and
IL-10.The Th1cytokinesboost cell-mediatedimmunity,and the
Th2 cytokines augment humoral immunity. IFN-
plays a criti-
cal role in the induction of other cytokines and in mediation of
macrophage and natural killer cell activation.
Several reports indicated thatconsumption ofyogurt orintake of
LAB by themselves modulatesthe productionof severalcytokines,
such as IL-1
, IL-6, IL-10, IL-12, IFN-
, and TNF-
(6063).
Moreover, the production of IFN-
in an in vitro culture system
using human lymphocytes was reported to be greater with cultures
in the presence of LAB (L. bulgaricus and S. thermophilus) than
with thosewithout LAB (64). Yogurt containing live L. bulgaricus
andS.thermophiluswasalsoreportedtoaugmentIFN-
production
by purified T cells from young adults after 4 mo feeding (62).
Effects of yogurt consumption on the modulation of cytokine
production in the human gastrointestinal tract, whether by cells
of the GALT or by others, have not been investigated. These
typesofstudies,although feasiblewiththe useof biopsysamples
from the intestines of healthy subjects (65), are difficult to carry
out, and good animal models currently do not exist.
248 ADOLFSSON ET AL
by guest on June 6, 2011www.ajcn.orgDownloaded from
Even though cytokines play diverse roles in regulating
immunefunctions, some cytokines, eg, IL-1
,IL-6, and TNF-
,
have been given more attention than others because they have
traditionally been classified as proinflammatory and as such are
known to be associated with inflammatory conditions such as
Crohndisease and ulcerativecolitis(66).Another diverse family
of immune modulators that play important roles in the health of
the gastrointestinal tractconsists of chemokinesand their recep-
tors(67).Currently,onlylimiteddatahavebeenpublishedonthe
effect of yogurt or its components on chemokine modulation in
the gastrointestinal tract. The effects of different strains of Lac-
tobacillus on chemokine production by the intestinal epithelial
cell-line, HT-29, were investigated by Wallace et al (68). All 3
LAB species investigatedL. acidophilus, Lactobacillus rham-
nosus, and Lactobacillus delbrueckiihad suppressive effects
on the production of 2 chemokines, RANTES (a member of the
IL-8 superfamily of cytokines) and IL-8, by activated HT-29
cells. As is the case with proinflammatory cytokines, these che-
mokines are necessary for normal immune function. However, a
high production of these chemokines during an inflammatory
condition is believed to exacerbate the inflammatory response.
Laxation
Few reports have discussed the effects of yogurt and LAB on
laxation. In the studies published, however, both significant ef-
fects (G Wilhelm, unpublished observations, 1993; 69) and no
effects (70) of yogurt or LAB on laxation and gastrointestinal
transit time were described.
Strandhagen et al (69) reported that the transit time for 50%
(t50)ofgastriccontentwassignificantlygreaterforropymilk,an
L. bulgaricus and S. thermophilusfermented milk product
indigenoustoSweden,thanforunfermentedmilk.Anotherstudy
showedthatmilkfermentedwithL.bulgaricusandS.thermophi-
lusreducedintestinaltransittimeinhumansubjectswithhabitual
constipation (G Wilhelm, unpublished observations, 1993). In
the same study, subjects consuming fermented milk also had
improved bowel function. The number of defecations increased
from 3/wk during a control period to 7/wk when fermentedmilk
was consumed. When milk fermented with L. acidophilus was
consumed,thenumberofdefecationsincreasedfurther to15/wk.
Studieswere conductedofthe effectsofacommercially avail-
able yogurt fermented with B. animalis on orofecal gut transit
time (71, 72). In a double-blind, randomized, crossover design,
B. animalis reduced the colonic transit time in a group of healthy
women aged 1845 y (72). Likewise, in a group of elderly
subjects experiencing lengthy orofecal gut transit time but oth-
erwise free of any gastrointestinal pathology, B. animalis intake
provided led to a significant reduction in transit time (71).Thus,
the effect of LAB ingestion on orofecal gut transit time appears
to be dependent on the bacterial strain used and the population
being studied.
YOGURT AND DISEASES OF THE
GASTROINTESTINAL TRACT
Lactase deficiency and lactose maldigestion
Lactase deficiency among adults is the most common of all
known enzyme deficiencies. More than half of the worlds adult
populationislactoseintolerant.Indevelopmentalterms,thismay
not necessarily be considered abnormal, because humans are the
only known mammal in whom lactase activity in the small
intestine is sustained after weaning. In the case of lactose mal-
digestion, undigested lactose remains in the intestinal lumen,
and, as it reaches the colon, it is fermented by colonic bacteria.
Byproductsofthisprocessincludeshort-chainfattyacidssuchas
lactate, butyrate, acetate, and propionate. These fatty acids as-
sociate with electrolytes and lead to an osmotic load that can
inducediarrhea. Furthermore,fermentationof lactosebycolonic
bacteriaproducesmethane,hydrogen,andcarbondioxide.These
gasesmay stay in the lumen and eventually will both be excreted
as flatus, diffusing into the circulation, and be exhaled via the
lungs. Exhaled hydrogen after a lactose load has been used asan
indirect but measurable indicator of lactose maldigestion. In
addition to lactose, some sources of dietary fiber and other un-
absorbed carbohydrates can serve as substrates for colonic fer-
mentation that results in increased hydrogen production.
Inability to digest lactose varies widely among ethnic and
geographic populations (73, 74). In the United States, the prev-
alence of primary lactose intolerance in adults is 53% among
Mexican Americans, 75% among African Americans, and 15%
among whites. The prevalence among adults in South America
and Africa is 50% and that in some Asian countries is close to
100%. Lactose intolerance varies greatly between European
countries, from 2% prevalence in Scandinavian adults to
70% among Southern Italian adults (74).
Lactosemaldigestionmaydevelopsecondarytoinflammation
orasaresultoffunctionallossofthesmallintestinalmucosa(14),
which can result from conditions such as Crohn disease, celiac
sprue, short bowel syndrome, or bacterial and parasitic infec-
tions. In addition, lactose maldigestion may develop as a conse-
quence of severe protein calorie malnutrition. The disorder is
clinically expressed by symptoms of abdominal cramps, diar-
rhea,andflatulenceaftermilkingestion.However,mostpersons
who have symptoms of lactose intolerance can endure small
amounts (210 g) of lactose in a meal without becoming symp-
tomatic (14).
It is well known that, for many lactose-intolerant people, fer-
mented milk products are better accepted than are unfermented
milk products. There may be more than one reason for this.
During fermentation of milk, lactose is partially hydrolyzed,
whichresultsinalowerlactosecontentinyogurtthaninmilk(2).
However, this reduction in lactose may not be significant, be-
cause milk solids are usually added during processing. The
greater tolerance of lactose from yogurt than of that from milk
among lactose-intolerant subjects may be due to the endogenous
lactaseactivity ofyogurtorganisms(13,15, 75).Kolarsetal(15)
used a series of breath hydrogen tests as well as a subjective
assessment to ascertain whether subjects who were identified as
lactose-intolerant digested and absorbed lactose in yogurt better
than they digested and absorbed lactose in milk. The area under
thecurve forbreathhydrogen wassmallerafteryogurt consump-
tion than after consumption of milk or lactose in water, which
indicates better digestion and absorption of lactose from yogurt
than of that from either milk or lactose in water. Subjective
assessment by the subjects in the study of Kolars et al also
indicatedthatlactoseinyogurtwasbettertoleratedthanthesame
amount of lactose from milk or in water. Using breath hydrogen
measurement, Savaiano et al (75) investigated the effects of 3
varieties of cultured milk products on the digestion of lactose by
9 lactase-deficient human subjects. When yogurt, cultured milk
(buttermilk),and sweet acidophilus milk were compared, yogurt
YOGURT AND GUT FUNCTION 249
by guest on June 6, 2011www.ajcn.orgDownloaded from
had the most beneficial effect on lactose digestion in these sub-
jects. Lactase activity and the number of surviving LAB were
significantly reduced when the yogurt was pasteurized.
The enzyme activity of lactase is generally stable in response
toenvironmentalfactors.Forexample,itwasshownthatthelactase
activityofyogurtwaspreservedandevenincreasedwhentheyogurt
was subjected to an environment that simulated the temperature
and low pH valuesof the gut (15).As suggestedby theauthors, this
study supports the notion that lactose in yogurt is autohydrolyzed
once it is in the jejunal environment. Other studies reported that
lactase activity is less stable in response to acidic environment.
Pochartetal(76)reportedthatlactaseactivityinyogurtdecreasedby
80% at a pH of 5.0 in an in vitro model.
However, heating yogurt does significantly decrease lactase
activity, which indicates that yogurt that has been heat treated is
not as beneficial for lactose-intolerant persons is yogurt contain-
ing live and active cultures. Thus, there is a growing body of
evidence that yogurt containing live and active cultures is better
tolerated by lactose malabsorbers than are heat-treated fer-
mented milks (50). During the fermentation process, the amount
of lactose present in yogurt is reduced. The lactose content also
varieswiththedurationofstorageafterfermentation.Inaddition,
thebacteriallactaseactivitycorrespondswiththesurvivaltimeof
lactobacilli after ingestion. The enhanced digestion of lactose is
explained partly by the improved lactase activity after yogurt
ingestion and partly by other enzymatic functions, such as the
activity of the lactose transport system (permease) that allows
lactose to enter the probiotic cell (77, 78). Furthermore, animal
studies have suggested that LAB may induce lactase activity of
the gut intestinal endothelial cells (79).
A study by Martini et al (80) supports the microbial mediation
of lactase activity in the gastrointestinal tract. Those authors
showed that lactase activity in yogurt was stable at pH 4.0, but
that microbial cell disruption resulted in 80% loss of lactase
activity and a twofold increase in lactose malabsorption in a
group of lactose maldigesters.
Although the organisms that make up the live cultures in
yogurtarerecognizedashavingfunctionallactaseactivityandas
contributing to the digestion of lactose, their survival in the
gastrointestinal tract is short. On average, significant numbers
survive for 1 h after ingestion (15, 50). Regardless of this
somewhat limited survival time, the beneficial effectof LAB on
lactose digestion in those suffering from lactose intolerance is
now widely accepted.
Diarrheal diseases
Diarrheaisacommonproblemamongchildrenworldwideand
has been reported to contribute substantially to pediatric physi-
cian visits and hospitalizations in the United States (81). Since
theearly20thcentury,ithasbeenhypothesizedthatlivebacterial
cultures, such as those used for the fermentation of dairy prod-
ucts, may offer benefits in preventing and treating diarrhea (4).
A recent meta-analysis of randomized, controlled studies by
VanNeilet al (82) found thattherapyusingLactobacillus strains
offered a safe and effective means of treating acute infectious
diarrheainchildren.Boththedurationandfrequencyofdiarrheal
episodes were reduced when compared with those in control
subjects. The benefit ofLactobacillus therapy was seen indiarrheal
diseases caused by various pathogens. The effect of supplementing
formulawithB.bifidumandS.thermophilusonpreventingtheonset
of acute viral diarrhea in infants was examined in a double-blind,
placebo-controlledtrial(83).Theinfantsreceivingbacterialtherapy
developed diarrhea and shed rotavirus less than did the infants fed
thecontrol formula. Evidenceofthe beneficial effectofLABon the
occurrence of diarrhea of bacterial origin is more contradictory be-
cause both benefits (84, 85) and noeffects (86,87) of feeding LAB
were reported.
Severalstudiesinvestigatedtheeffectsofprobioticbacteriaon
diarrhea associated with the use of antibiotics. The most likely
cause of diarrhea associated with antibiotic use is the negative
influence of antibiotics on the bacterial steady state of the intes-
tines (88). Most cases of antibiotic-associated diarrhea are mild,
and they end shortly after antibiotic therapy is discontinued. A
less common but more serious type of antibiotic-associated di-
arrhea is due to antibiotic-mediated overgrowth of pathogenic
bacterial species such as Clostridium difficile that is associated
with pseudomembranous colitis (89).
A recent meta-analysis evaluated the ability of several differ-
ent probiotic LAB species to prevent antibiotic-associated diar-
rhea (90). Of the 9 studies that were included in the analysis, 4
used Lactobacilli strains or a combination of Lactobacilli and
Bifidobacteria (9194). Of those 4 studies, 2 showed a signifi-
cantbenefitofprobioticuseincomparisonwithplacebo(93,94).
The authors concluded that probiotic bacteria supplied in cap-
sules or as yogurt-based products may be useful in preventing
antibiotic-associated diarrhea. However, none of these studies
provide evidence for a role of probiotic bacteria in the treatment
of such diarrhea.
The mechanisms by which LAB may provide a beneficial
effect against some forms of diarrheal disease are unknown. It
has been suggested that the beneficial effect may stem from the
abilityofLABtoreestablishtheintestinalmicroflora,toincrease
the intestinal barrier by competing with pathogenic bacteria for
adhesionto the enterocytes, or to increase mucosal IgA response
to pathogens.
Colon cancer
AccordingtotheNationalCancerInstitute,cancerofthecolon
is the second leading cancer diagnosis among both women and
men in the United States (95). Colon cancer is also the second
most common cause of cancer death. Risk factors for colorectal
cancer include both genetic and environmental factors, and sev-
eral reports have suggested that interactions between dietary
factors, colonic epithelium, and intestinal flora are central to the
development of colon cancer.
Theroleofdietintheetiologyof cancerhasbeengivengreater
attention in recent years. Although the relation between colon
cancer and certain food constituents, such as fiber and fat, gen-
eratedthemostinterest,thepossibilitythatfermenteddairyprod-
ucts may protect against tumor formation in the colon was also
investigated. Epidemiologic evidence suggests a negative corre-
lation between the incidence of certain cancers, including colon
cancer, and the intake of fermented dairy products (96). More-
over, fermented dairy products or the bacteria used for milk
fermentation were shown to have an effect on colon cancer and
certain other tumors in murine models of carcinogenesis (97
100). However, a number of animal studies investigating the
effectofvarious strains of LAB on colon carcinogenesis showed
inconsistent results.
Wollowskietal(100)investigatedtheprotectiveeffectofseveral
strains of LAB, traditionally used for milk fermentation, against
1,2-dimethylhydrazine (DMH)induced colon carcinogenesis in
250 ADOLFSSON ET AL
by guest on June 6, 2011www.ajcn.orgDownloaded from
rats. Oral treatment with L. bulgaricus for 4 d protected against
DMH-induced DNA damage in the colon. In contrast, there was no
protective effect when S. thermophilus was administered. The au-
thors did not ascertain the mechanisms of protection by L. bulgari-
cus,buttheyspeculatedthatthiol-containingbreakdownproductsof
proteinsthatresultfromtheproteolyticactivityofL.bulgaricusmay
have produced the effect.
InapreviousstudyusingasimilarDMH-inducedcoloncancer
model in rats, Shackelford et al (99) showed that milk fermented
with L. bulgaricus resulted in greater survival than did nonfer-
mented milk. However, in contrast to the findings of Wollowski
et al (100), L. bulgaricus-fermented milk did not reduce the
number of rats that developed colon tumors, whereas S.
thermophilus-fermented milk did do so (99). In a study using
azoxymethane to induce aberrant crypt foci in the colon of rats,
no significant effects were seen with either B. longum or L. casei
(101).Thoseauthorsdid,however,observeaprotectiveeffectof
L. acidophilus and inulin, but only when the total fat content of
the diet was increased.
Using a colon carcinoma cell culture system, Ganjam et al
(102) isolated a yogurt fraction that decreased cell proliferation,
as ascertained with the use of thymidine incorporation. Cell pro-
liferation was not inhibited in response to a similarly isolated
milk fraction or to lactic acid.
Elevated activity of several bacterial fecal enzymes, some of
which are involved in the metabolism of genotoxic nitrates, was
associatedwithanincreasedrisk of colon cancer (103, 104). The
activity of these enzymes can be altered by diet or antibiotic
intake (10, 105). L. acidophilus (106) and L. gasseri (43) were
shown to reduce the fecal enzyme activity of nitroreductase,
azoreductase, and
-glucuronidase in humans, with a reduction
by50% or 75% in the activities of these enzymes during a period
of Lactobacilli feeding. Likewise, Guerin-Danan et al (46) re-
ported that 1018-mo-old infants fed yogurt fermented with S.
thermophilus, L. bulgaricus, and L. casei had lower fecal
-glucuronidase activity than did a similar group of infants fed
milk or yogurt not fermented with L. casei.
The mechanism by which LAB may have an effect on colon
carcinogenesis is currently unknown. Some of the mechanisms
thatmaybeinvolvedincludeenhancementofthehostsgutimmune
response, suppression of harmful intestinal bacteria, sequestration
of potential mutagens, production of antimutagenic compounds,
reduction of pH concentrations in the colon, and alteration of other
physiologicconditions(107).Furthermore,itwasshownbyPedrosa
et al (43) that the feeding of yogurt or Lactobacillus reduced fecal
enzymes, which convert procarcinogens to carcinogens, such as
azoreductase and nitroreductase.
Inflammatory bowel disease
Inflammatory bowel disease (IBD) is a term used for certain
chronic immunemediated conditions of the intestinal tract.
These chronic diseases include Crohn disease and ulcerative
colitis,conditionsthathavecomparablesymptomsbutthataffect
the digestive tract in very different ways (66). Ulcerative colitis
involvesinflammationofthecolonandrectumandnotthatofthe
uppergastrointestinaltract,whereas Crohndiseasecanaffectthe
upperintestinaldigestivetractandthuscanleadtomalabsorption
of both macronutrients and micronutrients. The etiologies of
thesediseasesareunknown,butstudiessuggestthattheintestinal
microflora play a crucial pathogenic role (108). This notion is
supported by animal models of Crohn disease, in which the
presence of intestinal microflora is absolutely required for the
development of disease.
Proinflammatory cytokines, particularly TNF-
, have also
been recognized as playing a central role in the pathogenesis of
Crohn disease. However, despite earlier hopes, the results from
studies using TNF-
antagonists were disappointing, and there
were some reports of severe complications (109). Nevertheless,
reducing the production or effect of TNF-
(or both) in Crohn
disease patients is belived to be beneficial. Bourrel et al (63)
reported that, when inflamed intestinal mucosa from a group of
Crohns disease patients was cocultured in the presence of L.
casei or L. bulgaricus, expression and release of TNF-
by
intraepithelial lymphocytes were reduced.
Normally, a healthy mucosal barrier provides a first defense
mechanism against both the intestinal microflora and invading
pathogens.Ithasbeensuggestedthattheproportionsofdifferent
intestinal microflora are altered in patients with IBD. For exam-
ple, colonic biopsyspecimens have shown lower concentrations
of Lactobacillus and lower fecal concentrations of both Lacto-
bacillus and Bifidobacteriumspecies in patients with Crohn dis-
easethan in healthy subjects (110). This disturbance in intestinal
flora may increase the opportunity for colonization of pathogens
and bring about a subsequent proinflammatory response.
In the case of IBD, a defective mucosal barrier allows for in-
creased uptake of antigens and proinflammatory mediators origi-
nating from luminalbacteria. It hasbeen reported that patients with
IBDhavediminishedmucosalprotectionasaresultofchangesinthe
compositionandthicknessofthemucosallayerandalterationsinthe
glycosylationstatusofmucosalglycoproteins(111).These changes
intheintestinalmucosaarealsoassociatedwithdecreasedintestinal
IgA activity and increased IgG activity, which coincides with re-
duced state of protection and a proinflammatory condition. With
weakened mucosal barrierand therebyincreased adherence ofbac-
terial pathogens to the mucosa,sustained inflammation results, and
that leads to further damage to the gut mucosa. In recent years,
immunosuppressive and immunomodulating therapies, such as the
steroidsusedsincethe1960s,havebecome moreandmorefrequent
in the treatment of these conditions. Although efficacious, these
types of drugs can increase the prevalence of opportunistic infec-
tions as wellas the severityof any underlyinginfection that maybe
present (112). Other side effects of these treatments may include
hepatotoxicity, fibrosis, lymphoma, and pathologic suppression of
bone marrow function.
Theroleofbeneficialintestinalmicroflorainthepreventionof
intestinal inflammation was investigated by using gene-targeted
IL-10 knockout (IL-10
Ҁ/Ҁ
) mice (113, 114). These IL-10defi-
cient mice spontaneously develop ileocolitis with many similar-
ities to Crohn disease in humans. Furthermore, affected mice
respond favorably to immunosuppression or immunomodula-
tory drugs thatare similar tothose used to treathuman IBD. The
immunoregulatory activity of IL-10 has been studied exten-
sively. It is now well established that IL-10 plays a role in down-
regulating both the synthesis of inflammatory cytokines and
the presentation of antigens. Thus, IL-10 has been suggested for
use as an immunomodulator for the treatment of Crohn disease.
Targeted in vivo delivery of IL-10 to the affected intestinal ep-
ithelium by using genetically engineered Lactococcus lactis has
shown great promise in 2 mouse models of IBD (114).
Madsen et al (113) found that IL-10
Ҁ/Ҁ
mice had increased
adherence of luminal bacteria to the mucosal layer in the colon
YOGURT AND GUT FUNCTION 251
by guest on June 6, 2011www.ajcn.orgDownloaded from
that preceded the development of colitis. This occurred in par-
allel to decreased numbers of luminal Lactobacillus. When the
concentrations of Lactobacillus in the gastrointestinal lumen
were restored by rectal delivery of Lactobacillus reuteri or by
orallactulose therapy,colitiswas attenuated.Theconcentrations
of adherent and translocated bacteria in the mucosal wall also
were reduced.
Another benefit of LAB in Crohn disease may be due to the
stimulation of the IgA response. A report by Malin et al (115)
suggests that oral bacteriotherapy using L. casei can restore
antigen-specific IgA immune response in persons with Crohn
disease. In a previous study from the same laboratory (116), oral
administration of L. casei to patients with viral gastroenteritis
promoted antigen-specific IgA responses and shortened the pa-
tient diarrhea.
Although experimental evidence exists indicating beneficial
effects of LAB on Crohn disease and ulcerative colitis, the exact
mechanism through which LAB species antagonize the progres-
sionof these diseasesispoorlyunderstood. The exactetiologyof
IBD is also unknown, but it is likely that, in susceptible persons,
IBDresultsfromanongoinginflammatoryresponse,whichmay
be due to a defect in both the regulation of the mucosal proin-
flammatory response and the function of the intestinal epithe-
lium. Currently, evidence suggests that yogurt and LAB have
modestclinicalbenefitsandaresafe foruse inpatients withthese
conditions. Further studies are required to ascertain whether yo-
gurt is beneficial as a prophylactic or a therapeutic regimen for
IBD (or both) and to establish exactly which mechanisms are
involved.
Helicobacter pylori
It has only been 20 y since Helicobacter pylori, a gram-
negative, spiral-shaped bacterium that is found in the gastric
mucous layer or adherent to the epithelial lining of the stomach,
was discovered (117). H. pylori relies on the ammonia-
producing surface protein urease for adherence and colonization
to the gastric epithelium. Urease allows H. pylori to survive by
neutralizing the acidic gastric environment (118). H. pylori pro-
duces catalase, which may play a role in protecting the bacteria
from free radicals that are released by activated leukocytes. H.
pylori infection is associated with a massive infiltration of neu-
trophils into the gastric wall and local production of IFN-
,
proinflammatorycytokineseg,TNF-
,IL-1
,and IL-6and
the chemokine IL-8.
Infection with H. pylori is now known to play a role in peptic
ulcer disease, chronic gastritis, gastric adenocarcinoma, and
mucosa-associated lymphoid tissue lymphoma. The association
between duodenal ulcer disease and H. pylori is also well doc-
umented: H. pylori infection is reported in 90% of duodenal
ulcer patients (119). Treatment of this infectioninvolves the use
ofproton pump inhibitors, often in combination with antibiotics.
However, the use of antibiotics to treat H. pylori infection has
been associated with adverse effects and frequently leads to
resistance to antibiotic therapy.
Several in vitro and animal studies have shown reduced via-
bility of H. pylori and less adhesion of the bacteria to human
intestinal mucosal cells after treatment with various Lactobacil-
lus strains (120). In series of in vitro assays, Midolo et al (121)
showed that the growth of H. pylori was inhibited by lactic acid
in a pH-independent manner. They also found that 6 strains of L.
acidophilus and L. casei inhibited the growth of H. pylori,
whereas B. bifidus and L. bulgaricus did not. The inhibitory
effect correlated with the concentrations of lactic acid produced
by the LAB examined. In another study, Coconnier et al (122)
reported that conditioned media from L. acidophilus reduced the
viability of H. pylori in vitro, independent of lactic acid concen-
trations.In addition, the adhesion of H. pylorito human mucose-
cretingHT-29 cells decreased. Several in vitro studies were con-
ducted to ascertain whether the effects of LAB on H. pylori
survival and function are due to lactic acid or to other antibac-
terial products generated by LAB, such as bacteriocins. Of the
several bacteriocins tested, lacticins produced by Lactoc. lactis
were shown to have the greatest anti-Helicobacter activity when
used against several strains of H. pylori (123).
Studies that indicate promising inhibitory effects of LAB on H.
pylorisurvivalandfunctioninvitrowereextendedtoinvivostudies
using human patients. Armuzzi et al (124) reported that, when 120
asymptomatic subjects who were positive for H. pylori infection
received an L. casei strain GG supplement over a 14-d period in
addition to astandard 1-wkantibiotic therapy regimen,the eradica-
tion of H. pylori was faster than that in control subjects.
Although promising results have been reported, the effects of
LAB on H. pylori infection in humans remain ambiguous. For
example, L. acidophilus and L. gasseri were both shown to
decrease H. pylori infection, as indicated by reduced [
13
C] urea
breathtestvalues(125,126),andtherapywithL.acidophiluswas
shown to reduce gastric mucosal inflammation (125). However,
gastric biopsies did not show eradication of H. pylori. Similarly,
Cats et al (127) reported that viable L. casei was required to
inhibit the growth of H. pylori in vitro, but only a slight nonsig-
nificant trend was observed toward an in vivo suppressive effect
of an L. casei-supplemented milk drink.
Allergic reactions
The effects of yogurt and LAB on allergic reactions in the
gastrointestinal tract have received some interest (128, 129). It
was reported that a delay in the development of Bifidobacterium
and Lactobacillus in the gastrointestinal microflora is a general
finding in children with allergic reactions (128). Isolauri (130)
reported data suggesting that Lactobacillus GG can be used to
prevent food allergies.
Heat treatment was suggested as a way of reducingthe ability
of milk proteins to cause allergic reactions, which would make
milk a more suitable source of protein for persons with an im-
munologic sensitization to cow milk protein (131). However,
Kirjavainenetal(129)usedarandomizeddouble-blinddesignto
investigate in a recent study the effects of heat-inactivated and
viable L. rhamnosus GG on infants with atopic eczema and cow
milk allergy. Milk formula supplemented with viable but not
heat-inactivatedL.rhamnosusGGsignificantlyimprovedatopic
eczemaandsubjective symptoms of cow milk allergyinsubjects
in comparison with the control group. These results suggest that,
in persons with cow milk allergy, the presence of viable LAB
may provide benefits that outweigh the possible detrimental
effects that undenatured milk proteins may have on milk al-
lergy. Furthermore, the immunologic response to native milk
proteins may differ from that to heat-denatured milk proteins. A
recent study using a rat model showed that heat-denaturated
-lactoglobulininducedalocalmucosalinflammatoryresponse,
whereas native
-lactoglobulin induced an IgE-mediated
systemic response (132). Heat denaturation is likely to result in
252 ADOLFSSON ET AL
by guest on June 6, 2011www.ajcn.orgDownloaded from
conformational changes that expose or hide (or both) epitopes
and lead to the activation of different subpopulations of immune
cells and thus to different end results.
The mechanisms of the protective effects of LAB on allergic
reactions are not known. A proinflammatory response in the gut
mucosathatisinducedbyfoodallergensmayimpairthefunction
of the intestinal barrier. It is possible that LAB may prevent
allergic reactions by having a protective effect on the function of
theintestinal barrier,althoughthemechanismof suchaneffectis
poorly understood. A more direct link between the function of
GALTandallergicresponsesisalsopossible.Oneoftheprimary
mechanisms of active cellular suppression of proinflammatory
events in the gut after antigen-specific triggering is the secretion
of suppressive cytokines, such as transforming growth factor
and IL-10. Transforming growth factor
is produced by both
CD4
ѿ
and CD8
ѿ
GALT-derived T cells and is an important
mediator of the active suppression component of oral tolerance.
Furthermore,IL-4mediated isotype switching ofimmunoglob-
ulin from IgM to IgE and IgE-dependent degranulation of mast
cells has been shown to be involved in the pathogenesis of food
allergyrelated enteropathy (133).
Yogurts LAB are known to enhance the production of IFN-
(62, 134), which acts to inhibit isotype switching to IgE. IgE-
mediatedhypersensitivity reaction,alsoknown astype1 allergy,
is triggered by the cross-linking of antigens with IgE antibodies
that are bound to Fc receptors on mast cells. It was reported that
L. casei inhibited antigen-induced IgE production by mouse
splenocytes (135). In addition, production of the immunosup-
pressive cytokine IL-10 is induced by LAB (60).
A combination of enhancing and suppressive effects is the
most likely mechanism by which LAB may have their effects.
However,the ways inwhichLABor other componentsofyogurt
influencetheproductionoftheseimmunoregulatorycytokinesin
thegut remaintobeelucidated,as dothepossiblemechanismsof
LAB-mediated protection.
SAFETY
Although the safe use of nonsporing anaerobic LAB in fer-
mented foods is widespread and has a long history, there have
beenoccasional reports associating LAB with clinical infections
(53,136)becausebenignmicroorganismshavebeenshowntobe
infective when a patient is severely debilitated or immunosup-
pressed (137, 138). Some of the diseases that have been associ-
ated with LAB infection include septicemia, infective endocar-
ditis, and dental caries.
Very rarely, cases of lactobacillemia have been reported in
patients with severe underlying illness, many of whom received
a prior antibiotic therapy that may have selected-out for the
organism (139, 140). Moreover, Husni et al (141) reviewed the
cases of 45 patients with clinically significant lactobacillemia
and reported that 11 of the patients were receiving immunosup-
pressivetherapyand23 hadreceivedantibiotics. Innone ofthese
reports was a definitive link made between the consumption of
fermented milk products and infection.
In addition, rare cases of endocarditis have been associated
with L. rhamnosus, a LAB indigenous to the human gastrointes-
tinal tract (142144). However, as with lactobacillemia, no re-
ports to date have been able to identify a connection between
LAB from fermented milk and infection in humans. In most of
thesecases,theoriginoftheLactobacillusismostlikelythehost.
There is also a hypothetical risk of the transfer of antimicrobial
resistance from LAB to other microorganisms with which LAB
might come in contact, but this has not yet been described in the
literature.
In the past, Lactobacilli isolated from infections were habit-
uallydismissedas contaminants or secondary invaders. However,
recent evidence suggests that they might function as opportunistic
pathogens in a small number of severely immunosuppressed
persons.Eveninthesepatients,thisisaveryrareevent,andithas
not yet been reported in a large group of immunosuppressed
persons, such as the elderly or persons with AIDS. LAB have a
long history of safe use in foods and also in products that have
been tested in clinical trials. However, as with any new food
ingredient, the safety of a new strain of LAB must be clearly
establishedbeforeitisintroducedintofermenteddairyproducts.
CONCLUDING REMARKS AND RECOMMENDATIONS
FOR FUTURE STUDIES
It has long been believed that the consumption of yogurt and
other fermented milk products provides various health benefits.
Recent studies of the possible health benefits of yogurt in gut-
associated diseases substantiate some of these beliefs. Of partic-
ular interest are the reductionby yogurt, yogurt bacteria, or
bothin the duration of diarrheal diseases in children, the pre-
ventive or therapeutic (or both) effects on IBD and colon cancer
as suggested by epidemiologic evidence and animal studies, and
thepossiblebeneficialeffectsinincreasingtheeradicationrateof
H. pylori as indicated by in vitro and preliminary human studies.
In addition, there is ever-increasing evidence of the beneficial
effect of yogurt containing live and active cultures on the diges-
tion of lactose in persons with lactose intolerance.
These findings are interesting and should encourage future
studiesto1)substantiateorextendthesefindingsbyusinganimal
models and clinical trials; 2) ascertain whether these effects are
age-specific or can be observed across all age groups: eg, ascer-
tainwhetheryogurt would have effects similar to those observed
in children on attenuation of the incidence or duration of diar-
rheal diseases in elderly people, a group that has high morbidity
andmortalityfrom these infections; and 3) investigate the mech-
anisms through which yogurt exerts its effects and ascertain the
critical components of yogurt involved in its mechanisms of
action. Finally, in recent years, yogurt has been touted as im-
proving gut health. In the absence of a universally accepted
definition or any definition of gut health,it is difficult to sub-
stantiate these claims. Studies focused on determining the char-
acteristics of a healthy gut would be extremely helpful in eval-
uating the effect of yogurt on gut health.
All 3 authors participated in the literature review and the development of
the manuscript outline, and SNM and RMR determined the areas to be
discussed. OA conducted the literature search and organized and wrote the
manuscript. SNM provided corrections. RMR revised the manuscript.
This review was prepared in response to a request from the National
Yogurt Association fora critical and objectivereview, for which theauthors
received an honorarium.
REFERENCES
1. Guarner F, Schaafsma GJ. Probiotics. Int J Food Microbiol 1998;39:
2378.
2. Bourlioux P, Pochart P. Nutritional and health properties of yogurt.
World Rev Nutr Diet 1988;56:21758.
YOGURT AND GUT FUNCTION 253
by guest on June 6, 2011www.ajcn.orgDownloaded from
3. Chandan RC,Shahani KM. Yogurt. In: Hui YH, ed. Dairy science and
technology handbook. New York: VCH Publishers, Inc, 1993:157.
4. MetchnikoffE.Sur lafloreducorpshumain.(Onthefloraofthehuman
body. ) Manch Lit Philos Soc 1901;45:138 (in French).
5. Perdigon G, Alvarez S, Rachid M, Aguero G, Gobbato NJ. Immune
system stimulation by probiotics. J Dairy Sci 1995;78:1597606.
6. ButtrissJ.Nutritionalpropertiesoffermentedmilkproducts.IntJDairy
Tech 1997;50:217.
7. ReddyKP,ShahaniKM,KulkarniSM.B-complexvitaminsincultured
and acidified yogurt. J Dairy Sci 1976;59:1915.
8. Shahani KM, Chandan RC. Nutritional and healthful aspects of cul-
turedandculture-containingdairyfoods.JDairySci1979;62:168594.
9. Kneifel W, Mayer HK. Vitamin profiles of kefirs made from milks of
different species. Int J Food Sci Technol 1991;26:4238.
10. Kneifel W, Kaufmann M, Fleischer A, Ulberth F. Screening of com-
merciallyavailablemesophilicdairy starter cultures: biochemical, sen-
sory and morphological properties. J Dairy Sci 1992;75:315866.
11. Crittenden RG, Martinez NR, Playne MJ. Synthesis and utilisation of
folate by yoghurt starter cultures and probiotic bacteria. Int J Food
Microbiol 2003;80:21722.
12. Wigertz K, Svensson UK, Ja¨gerstad M. Folate and folate binding pro-
tein content in dairy products. J Dairy Res 1996;64:23954.
13. Rosado JL, Solomons NW, Allen LH. Lactose digestion from unmod-
ified,low-fatandlactose-hydrolyzed yogurt in adult lactose maldigest-
ers. Eur J Clin Nutr 1992;46:617.
14. Vesa TH, Marteau P, Korpela R. Lactose intolerance. J Am Coll Nutr
2000;19:165S75S.
15. Kolars JC, Levitt MD,AoujiM,SavaianoDA.Yogurtanautodigest-
ing source of lactose. N Engl J Med 1984;310:13.
16. Goodenough ER, Kleyn DH. Influence of viable yogurt microflora on
digestion of lactose by the rat. J Dairy Sci 1976;59:6016.
17. Rasic JL,Kurmann JA. Yoghurt: scientific grounds, technology, man-
ufacture and preparations. Vol 1 of Rasic JL, Kurmann JA, eds. Fer-
mented fresh milk products and their cultures. Copenhagen: Technical
Dairy Publishing House, 1978.
18. Loones A. Transformation of milk components during yogurt fermen-
tation. In: Chandan RC, ed. Yogurt: nutritional and health properties.
McLean, VA: National Yogurt Association, 1989:95114.
19. Beshkova DM, Simova ED, Frengova GI, Simov ZI, Adilov EF. Pro-
duction of amino acids by yogurt bacteria. Biotechnol Prog 1998;14:
9635.
20. Hewitt D, Bancroft HJ. Nutritional value of yogurt. J Dairy Res 1985;
52:197207.
21. Bissonnette DJ, Jeejeebhoy KN, eds. Meetingdietary nutrient require-
ments with cows milk and milk products. Rotterdam: Balkema, 1994.
22. Gaudichon C, Roos N, Mahé S, Sick H, Bouley C, Tomé D. Gastric
emptying regulates the kinetics of nitrogen absorption from
15
N-
labeled milk and
15
N-labeled yogurt in miniature pigs. J Nutr 1994;
124:19707.
23. Gaudichon C, Mahé S, Roos N, et al. Exogenous and endogenous
nitrogen flow rates and level of protein hydrolysis in the human jeju-
num after [
15
N] milk and [
15
N] yogurt ingestion. Br J Nutr 1995;74:
25160.
24. Shantha NC, Ram LN, OLeary J, Hicks CL, Decker EA. Conjugated
linoleic acid concentrations indairy products asaffected by processing
and storage. J Food Sci 1995;60:6958.
25. Aneja RP, Murthi TN. Conjugated linoleicacidcontentsof Indian curd
and ghee. Indian J Dairy Sci 1990;43:2318.
26. Jiang J, Wolk A, Vessby B. Relation between the intake of milk fat and
the occurrence of conjugated linoleic acid in human adipose tissue.
Am J Clin Nutr 1999;70:217.
27. Park Y, McGuire MK, Behr R, McGuire MA, Evans MA, SchultzTD.
High-fat dairy product consumption increases 9c;11t18:2 (rumenic
acid) and total lipid concentrations of human milk. Lipids 1999;34:
5439.
28. Boccignone M, Brigidi R, Sarra C. Studi effettuati sulla compo-sizione
in trigliceridi ed acidi grassi liberi nello yogurt preparato dalatte vac-
cino, pecorinoe, caprino. (Studies on triglyceride and free fatty acid
composition of yogurt prepared from cow, goat, and sheep milk.) Ann
Fac Med Vet (Torino) 1984;28:22333 (in Italian).
29. Whigham LD, Cook ME, Atkinson RL. Conjugated linoleic acid: im-
plications for human health. Pharmacol Res 2000;42:50310.
30. KempMQ,JeffyBD,RomagnoloDF.Conjugatedlinoleicacidinhibits
cell proliferation through a p53-dependent mechanism: effects on the
expression of G1-restriction points in breast and colon cancer cells. J
Nutr 2003;133:36707.
31. Block G, Abrams B. Vitamin and mineral status of women of child-
bearing potential. Ann N Y Acad Sci 1993;678:24454.
32. Ervin RB, Kennedy-Stephenson J. Mineral intakes of elderly adult
supplement and non-supplementusers in the third NationalHealth and
Nutrition Examination Survey. J Nutr 2002;132:34227.
33. Allen LH. Calciumbioavailability and absorption: areview. Am J Clin
Nutr 1982;35:783808.
34. KaupSM,ShahaniKM,AmerMA,PeoER.(Bioavailabilityofcalcium
in yogurt.) Milchwissenschaft 1987;42:5136 (in German).
35. SchaafsmaGJ,DekkerPR, deWardH.Nutritionalaspects ofyogurt.2.
Bioavailability of essential minerals and trace elements. Neth Milk
Dairy J 1988;42:13546.
36. Bronner F, Pansu D. Nutritional aspects of calcium absorption. J Nutr
1999;129:912.
37. Norman AW. Intestinal calcium absorption: a vitamin D-hormone
mediated adaptive response. Am J Clin Nutr 1990;51:290300.
38. Pointillart A, Cayron B, Gueguen L. Calcium and phosphorus utiliza-
tion and bone mineralization in yogurt-fed pigs. Sci Alim 1986;6:15
30.
39. Bernet MF, Brassart D, NeeserJR,Servin AL. Lactobacillus acidophi-
lus LA 1 binds to cultured human intestinal cell lines and inhibits cell
attachment and cell invasion by enterovirulent bacteria. Gut 1994;35:
4839.
40. Alm L, Pettersson L. Survival rate of lactobacilli during digestion: an
in vitro study Am J Clin Nutr 1980;33(suppl):S2543 (abstr).
41. Robins-Browne RM, Path FF, Levine MM. The fate of ingested lacto-
bacilli in theproximal small intestine. Am J ClinNutr 1981;34:5149.
42. ConwayPL,GorbachSL, GoldinBR.Survivaloflactic acidbacteriain
the human stomach and adhesion to intestinal cells. J Dairy Sci 1987;
70:112.
43. Pedrosa MC, Golner BB, Goldin BR, Barakat S, Dallal GE, Russell
RM. Survival of yogurt-containing organisms and Lactobacillus gas-
seri (ADH) and their effect on bacterial enzyme activity in the gastro-
intestinal tract of healthy and hypochlorhydric elderly subjects. Am J
Clin Nutr 1995;61:3539.
44. Clark PA, Martin JH. Selection of bifidobacteria for use as dietary
adjuvants in cultured dairy foods: III. Tolerance to stimulated bile
concentrations of human small intestines. Cult Dairy Prod J 1994;29:
1821.
45. Duez H, Pelletier H, Cools S, et al. A colony immunoblotting method
forquantitativedetectionofaBifidobacteriumanimalisprobioticstrain
in human faeces. J Appl Microbiol 2000;88:101927.
46. Guerin-Danan C, Chabanet C, Pedone C, et al. Milk fermented with
yogurt cultures and Lactobacillus casei compared with yogurt and
gelled milk: influenceon intestinal microflora inhealthy infants. Am J
Clin Nutr 1998;67:1117.
47. Bouhnik Y, Pochart P, Marteau P, Arlet G, Goderel I, Rambaud JC.
Fecal recovery in humans of viable Bifidobacterium sp ingested in
fermented milk. Gastroenterology 1992;102:8758.
48. Plant L, Conway P. Association of Lactobacillus spp. with Peyers
patches in mice. Clin Diagn Lab Immunol 2001;8:3204.
49. Bernet MF, Brassart D, Neeser JR, Servin AL. Adhesion of human
bifidobacterial strains to cultured human intestinal epithelial cells and
inhibition of enteropathogen-cell interactions. Appl Env Microbiol
1993;59:41218.
50. Lerebours E, N'Djitoyap Ndam C, Lavoine A, Hellot MF, Antoine JM,
ColinR.Yogurtand fermented-then-pasteurized milk: effects of short-
termandlong-termingestiononlactoseabsorptionandmucosallactase
activity in lactase-deficient subjects. Am J Clin Nutr 1989;49:8237.
51. Kankaanpa¨a¨ P, Salminen SJ, Isolauri E, Lee YK. The influence of
polyunsaturated fatty acids on probiotic growth and adhesion. FEMS
Microbiol Lett 2001;194:14953.
52. Kankaanpa¨a¨ P, Yang B, Kallio H, Isolauri E, Salminen S. Effects of
polyunsaturatedfattyacidsingrowthmediumonlipidcompositionand
on physicochemical surface properties of Lactobacilli. Appl Env Mi-
crobiol 2004;70:12936.
53. Aguirre M, Collins MD.Lactic acid bacteria andhuman clinical infec-
tion. J Appl Bacteriol 1993;75:95107.
54. Brandtzaeg P, Baekkevold ES, Farstad IN, et al. Regional specializa-
tion in the mucosal immune system: what happens in the microcom-
partments? Immunol Today 1999;20:14151.
55. Macpherson AJ, Gatto D, Sainsbury E, Harriman GR, Hengartner H,
254 ADOLFSSON ET AL
by guest on June 6, 2011www.ajcn.orgDownloaded from
Zinkernagel RM. A primitive T cell-independent mechanism of intes-
tinalmucosal IgAresponsestocommensal bacteria.Science2000;288:
22226.
56. Puri P,Rattan A, Bijlani RL, Mahapatra SC, Nath I. Splenic and intes-
tinal lymphocyte proliferation response in mice fed milk or yogurt and
challenged with Salmonella typhimurium. Int J Food Sci Nutr 1996;
47:3918.
57. Link-Amster H, Rochat F, Saudan KY, Mignot O, Aeschlimann JM.
Modulation of a specific humoral immune response and changes in
intestinal flora mediated through fermented milk intakes. FEMS Im-
munol Med Microbiol 1994;10:5564.
58. Perdigon G, de Macias ME,AlvarezS, Oliver G, de Ruiz HolgadoAA.
Systemic augmentation of the immune response in mice by feeding
fermented milks with Lactobacillus casei andLactobacillus acidophi-
lus. Immunology 1988;63:1723.
59. Mosmann TR, Cherwinski H, Bond MW, Giedlin MA, Coffman RL.
Two types of murine helper T cell clone. I. Definition according to
profiles of lymphokine activities and secreted proteins. J Immunol
1986;136:234857.
60. MiettinenM,Vuopio-VarkilaJ, VarkilaK.Productionof humantumor
necrosis factor-alpha, interleukin-6 and interleukin-10 is induced by
lactic acid bacteria. Infect Immun 1996;64:54035.
61. Solis-Pereyra B, Aattouri N, Lemonnier D. Role of food in the stim-
ulation of cytokine production. Am J Clin Nutr 1997;66(suppl):
521S5S.
62. Halpern GM, Vruwink KG, van de Water J, Keen CL, Gershwin ME.
Influence of long-term yogurt consumption in young adults. Int J Im-
munother 1991;7:20510.
63. Borruel N, Carol M, Casellas F, et al. Increased mucosal tumour ne-
crosisfactor alphaproductioninCrohnsdiseasecanbedownregulated
ex vivo by probiotic bacteria. Gut 2002;51:65964.
64. De Simone C, Bianchi Salvadori B, Negri M,Ferrazzi M, Baldinelli L,
Vesely R. The adjuvant effect of yogurt on production of gamma-
interferon by Con A stimulated human peripheral blood lymphocytes.
Nutr Rep Int 1986;33:41933.
65. Beharka AA, Paiva S, Leka LS, Ribaya-Mercado JD, Russell RM,
Nibkin Meydani S. Effect of age on the gastrointestinal-associated
mucosal immune response of humans. J Gerontol A Biol Sci Med Sci
2001;56:B21823.
66. Podolsky DK. Inflammatory bowel disease. N Engl J Med 2002;347:
41729.
67. AjueborMN,SwainMG.Roleofchemokinesandchemokinereceptors
in the gastrointestinal tract. Immunology 2002;105:13743.
68. Wallace TD, Bradley S, BuckleyND, Green-Johnson JM.Interactions
of lactic acid bacteria with human intestinal epithelial cells: effects on
cytokine production. Food Prot 2003;66:46672.
69. Strandhagen E, Lia A,Lindstrand S,et al.Fermented milk (ropymilk)
replacingregularmilkreducesglycemicresponceandgastricemptying
in healthy subjects. Scand J Nutr 1994;38:11721.
70. Nakamura T, Nishida S, Mizutani M, Iino H. Effects of yogurtsupple-
mented with brewers yeast cell wall on constipation and intestinal
microflora in rats. J Nutr Sci Vitaminol (Tokyo) 2001;47:36772.
71. Meance S, Cayuela C, Turchet P, Raimondi A, Lucas C, Antoine JM.
A fermented milkwith a Bifidobacterium probiotic strainDN-173 010
shortened oro-fecal gut transit time in elderly. Microb Ecol Health Dis
2001;13:21722.
72. Marteau P, Cuillerier E, Meance S, et al. Bifidobacterium animalis
strain DN-173 010 shortens the colonic transit time in healthy women:
adouble-blind,randomized,controlledstudy.AlimentPharmacolTher
2002;16:58793.
73. Rorick MH, Scrimshaw NS. Comparative tolerance of elderly from
differing ethnic backgrounds to lactose-containing and lactose-free
dairy drinks: a double-blind study. J Gerontol 1979;34:1916.
74. Sahi T. Geneticsand epidemiology of adult-type hypolactasia. Scand J
Gastroenterol 1994;202:720.
75. Savaiano DA, AbouElAnouar A, Smith DE, Levitt MD. Lactose mal-
absorption from yogurt, pasteurized yogurt, sweet acidophilus milk,
and cultured milk in lactase-deficient individuals. Am J Clin Nutr
1984;40:121923.
76. Pochart P, Dewit O, Desjeux JF, Bourlioux P. Viable starter culture,
-galactosidase activity, and lactose in duodenum after yogurt inges-
tion in lactase-deficient humans. Am J Clin Nutr 1989;49:82831.
77. HickeyMW,HillierAJ,JagoGR.Transportandmetabolismoflactose,
glucose,and galactose in homofermentativelactobacilli. Appl Environ
Microbiol 1986;51:82531.
78. Foucaud C, Poolman B. Lactose transport system of Streptococcus
thermophilus. J Biol Chem 1992;267:2208794.
79. Thoreux K, Balas D, Bouley C, Senegas-Balas F. Diet supplemented
with yoghurt or milk fermented by Lactobacillus casei DN-114 001
stimulates growth and brush-border enzyme activities in mouse small
intestine. Digestion 1998;59:34959.
80. Martini MC, Bollweg GL, LevittMD,Savaiano DA. Lactose digestion
byyogurt
-galactosidase:influenceof pHandmicrobialcell integrity.
Am J Clin Nutr 1987;45:4326.
81. Glass RI, Lew JF, Gangarosa RE, LeBaron CW, Ho MS. Estimates of
morbidity and mortality rates for diarrheal diseases in American chil-
dren. J Pediatr 1991;118:S2733.
82. VanNeilCW,FeudtnerC,GarrisonMM,ChristakisDA.Lactobacillus
therapy for acute infectious diarrhea in children: a meta-analysis. Pe-
diatrics 2002;109:67884.
83. SaavedraJM,BaumanNA,OungI,PermanJA,YolkenRH.Feedingof
Bifidobacterium bifidum and Streptococcus thermophilus to infants in
ahospitalforprevention of diarrhoea and shedding ofrotavirus.Lancet
1994;344:10469.
84. Gorbach SL, Chang TW, Goldin B. Successful treatment of relapsing
Clostridium difficile colitis with Lactobacillus GG. Lancet 1987;2:
1519(letter).
85. Biller JA, Katz AJ, Flores AF, Buie TM, Gorbach SL. Treatment of
recurrent Clostridium difficile colitis with Lactobacillus GG. J Pediatr
Gastroenterol Nutr 1995;21:2246.
86. Shornikova AV, Isolauri E, Burkanova L, Lukovnikova S, Vesikari T.
A trial in the Karelian Republic of oral rehydration and Lactobacillus
GG for treatment of acute diarrhoea. Acta Paediatr 1997;86:4605.
87. Clements ML, Levine MM, Ristaino PA, Daya VE, Huges TP. Exog-
enouslactobacillifedto mantheirfateandabilitytopreventdiarrheal
disease. Prog Food Nutr Sci 1983;7:2937.
88. Bartlett JG. Antibiotic-associated diarrhea. Clin Infect Dis 1992;15:
57381.
89. Van der Waaij D. The ecology of the human intestine and its conse-
quences for overgrowth by pathogens such as Clostridium difficile.
Annu Rev Microbiol 1989;43:6987.
90. DSouzaAL,RajkumarC,CookeJ,BulpittCJ.Probioticsinprevention
of antibiotic associated diarrhoea: meta-analysis. BMJ 2002;324:16.
91. Gotz V, Romankiewicz JA, Moss J, Murray HW. Prophylaxis against
ampicillin associated diarrhoea with Lactobacillus preparation. Am J
Hosp Pharm 1979;36:7547.
92. Tankanow RM, Ross MB, Ertel IJ, Dickinson DG, McCormick LS,
Garfinkel JF. A double blind, placebo-controlled study of the efficacy
of Lactinex in the prophylaxis of amoxicillin-induced diarrhea. DICP
1990;24:3824.
93. Orrhage K,Brismar B, Nord CE. Effects of supplements of Bifidobac-
terium longum and Lactobacillus acidophilus on intestinal microbiota
during administration of clindamycin. Microb Ecol Health Dis 1994;
7:1725.
94. Vanderhoof JA, Whitney DB, Antonson DL, Hanner TL, Lupo JV,
Young RJ. Lactobacillus GG in the prevention of antibiotic-associated
diarrhoea in children. J Pediatr 1999;135:35668.
95. National Cancer Institute. SEER Cancer Incidence Public-Use Data-
base, 1973-1996, August 1998 Submission. Bethesda, MD: US De-
partment of Health and Human Services, Public Health Service, 1999.
96. Peters RK, Pike MC, Garabrant D, Mack TM. Diet and colon cancer
in Los Angeles County, California. Cancer Causes Control 1992;3:
45773.
97. ReddyBS,RivensonA.InhibitoryeffectofBifidobacteriumlongumon
colon, mammary, and liver carcinogenesis induced by 2-amino-3-
methylimidazo[4,5-f]quinoline, a food mutagen. Cancer Res 1993;53:
39148.
98. Ayebo AD, Shahani KM, Dam R. Antitumor component(s) of yogurt:
fractionation. J Dairy Sci 1981;64:231823.
99. Shackelford LA, Rao DR, Chawan CB, Pulusani SR. Effect of feeding
fermentedmilkon the incidenceofchemicallyinducedcolon tumors in
rats. Nutr Cancer 1983;5:15964.
100. Wollowski I,Ji S, Bakalinsky AT, Neudecker C, Pool-Zobel BL. Bac-
teria used for the production of yogurt inactivate carcinogens and pre-
vent DNA damage in the colon of rats. J Nutr 1999;129:7782.
101. Bolognani F, Rumney CJ, Pool-Zobel BL, Rowland IR. Effect of
YOGURT AND GUT FUNCTION 255
by guest on June 6, 2011www.ajcn.orgDownloaded from
lactobacilli,bifidobacteriaandinulinontheformation ofaberrantcrypt
foci in rats. Eur J Nutr 2001;40:293300.
102. Ganjam LS, Thornton WH, Marshall RT, MacDonald RS. Antiprolif-
erative effects of yogurt fractions obtained by membrane dialysis on
cultured mammalian intestinal cells. J Dairy Sci 1997;80:23259.
103. Kim DH, Jin YH. Intestinal bacterial beta-glucuronidase activity of
patients with colon cancer. Arch Pharm Res 2001;24:5647.
104. Reddy BS, Engle A, Simi B, Goldman M. Effect of dietary fiber on
colonic bacterial enzymes and bile acids in relation to colon cancer.
Gastroenterology 1992;102:147582.
105. GoldinBR,GorbachSL.Alterationsoftheintestinalmicroflorabydiet,
oralantibiotics,andLactobacillus:decreasedproductionoffreeamines
from aromatic nitro compounds, azo dyes, and glucuronides. J Natl
Cancer Inst 1984;73:68995.
106. GoldinBR,GorbachSL.Theeffectofmilkandlactobacillusfeedingon
human intestinal bacterial enzyme activity. Am J Clin Nutr 1984;39:
75661.
107. Rafter JJ. The role of lactic acid bacteria in colon cancer prevention.
Scand J Gastroenterol 1995;30:497502.
108. Sartor RB. Pathogenesis and immune mechanisms of chronic inflam-
matory bowel diseases. Am J Gastroenterol 1997;92:5S11S.
109. KwonHJ,CoteTR, Cuffe MS,KramerJM,Braun MM. Casereportsof
heart failure aftertherapy with a tumor necrosisfactor antagonist. Ann
Intern Med 2003;138:80711.
110. FabiaR,ArRajabA,JohanssonML,etal.Impairmentofbacterialflora
inhuman ulcerativecolitisandexperimentalcolitisintherat. Digestion
1993;54:24855.
111. McCormick DA, Horton LW, Mee AS. Mucin depletion in inflamma-
tory bowel disease. J Clin Pathol 1990;43:1436.
112. van Wijngaarden P, Meijssen MA. Tuberculous pleurisy: an unusual
complication during treatment of Crohn disease with azathioprine.
Scand J Gastroenterol 2001;37:10047.
113. Madsen KL, Doyle JS, Jewell LD, Tavernini MM, Fedorak RN. Lac-
tobacillus species prevents colitis in interleukin 10 gene-deficient
mice. Gastroenterology 1999;116:110714.
114. Steidler L, Hans W, Schotte L, et al. Treatment of murine colitis by
Lactococcus lactis secreting interleukin-10. Science 2000;289:13525.
115. Malin M, Suomalainen H, Saxelin M, Isolauri E. Promotion of IgA
immune response in patients with Crohns disease by oral bacterio-
therapy with Lactobacillus GG. Ann Nutr Metab 1996;40:13745.
116. Kaila M, Isolauri E, Soppi E, Virtanen E, Laine S, Arvilommi H.
Enhancement of the circulating antibody secreting cell response in
human diarrhea bya human Lactobacillusstrain. Pediatr Res1992;32:
1414.
117. Marshall BJ. Unidentified curved bacillus on gastric epithelium in
active chronic gastritis. Lancet 1983;1:12735.
118. Labigne A, de Reuse H. Determinants of Helicobacter pylori patho-
genicity. Infect Agents Dis 1996;5:191202.
119. Duggan A. Helicobacter pylori: when is treatment now indicated? Int
Med J 2002;32:4659.
120. Aiba Y, Suzuki N, Kabir AMA, Takagi A, Koga Y. Lactic acid-
mediated supression of Helicobacter pylori by the oral administration
of Lactobacillus salivarius as a probiotic ina gnobiotic murine model.
Am J Gastroenterol 1998;93:2097101.
121. MidoloPD,LambertJR,HullR,LuoF,GraysonML.Invitroinhibition
of Helicobacter pylori NCTC 11637 by organic acids and lactic acid
bacteria. J Appl Bacteriol 1995;79:4759.
122. Coconnier M, Lievin V, Hemery E, Servin AL. Antagonistic activity
against Helicobacter infection in vitro and in vivo by the human
Lactobacillus acidophilus strain LB. Appl Env Microbiol 1998;64:
457380.
123. Kim TS, Hur JW, Yu MA, et al.Antagonism of Helicobacter pylori by
bacteriocins of lactic acid bacteria. J Food Prot 2003;66:312.
124. Armuzzi A, Cremonini F, Ojetti V, et al. Effect of Lactobacillus GG
supplementation on antibiotic-associated gastrointestinal side effects
duringHelicobacterpylorieradication therapy:apilotstudy.Digestion
2001;63:17.
125. Michetti P, Dorta G, Wiesel PH, et al. Effect of whey-based culture
supernatant of Lactobacillus acidophilus (johnsonii) La1 on Helico-
bacter pylori infection in humans. Digestion 1999;60:2039.
126. Sakamoto I, Igarashi M, Kimura K, Takagi A, Miwa T, Koga Y. Sup-
pressive effect of Lactobacillus gasseri OLL 2716 (LG21) on Helico-
bacter pylori infection in humns. J Antimicrob Chemother 2001;47:
70910.
127. Cats A, Kuipers EJ, Bosschaert MAR, Pot RGJ, Vandenbroucke-
Grauls CMJE, Kusters JG. Effect of frequent consumption of a Lacto-
bacillus casei-containing milk drink in Helicobacter pylori-colonized
subjects. Aliment Pharmacol Ther 2003;17:42935.
128. Kallioma¨ki M, Isolauri E. Role of intestinal florainthedevelopmentof
allergy. Curr Opin Allergy Clin Immunol 2003;3:1520.
129. Kirjavainen PV, Salminen SJ, Isolauri E. Probiotic bacteria in the
management of atopic disease: underscoring the importance of viabil-
ity. J Pediatr Gastroenterol Nutr 2003;36:2237.
130. Isolauri E. Studies on Lactobacillus GG in food hypersensitivity dis-
orders. Nutr Today 1996;31:28S31S.
131. Gurr MI. The nutritional role of cultured dairy products. Can Inst Food
Sci Technol 1984;17:5764.
132. Rytkönen J, Karttunen TJ, Karttunen R, et al. Effect of heat denatur-
ation on beta-lactoglobulin-induced gastrointestinal sensitization in
rats: denatured
LG induces a more intensive local immunologic re-
sponse than native
LG. Pediatr Allergy Immunol 2002;13:26977.
133. Bischoff SC, Mayer JH, Manns MP. Allergy and the gut. Int Arch
Allergy Immunol 2000;121:27083.
134. Miettinen M, Matikainen S, Vuopio-Varkila J, et al. Lactobacilli and
streptococci induce interleukin-12 (IL-12), IL-18, and gamma inter-
feron production in human peripheral blood mononuclear cells. Infect
Immun 1998;66:605862.
135. Shida K, Makino K, Morishita A, et al. Lactobacillus casei inhibits
antigen-induced IgE secretion through regulation of cytokine produc-
tion in murine splenocyte cultures. Int Arch Allergy Immunol 1998;
115:27887.
136. Gasser F. Safety of lactic acid bacteria and their occurrence in human
clinical infection. Bull Inst Pasteur 1994;92:4567.
137. MacGregor G, Smith AJ, Thakker B, Kinsella J. Yoghurt biotherapy:
contraindicated in immunosuppressed patients? Postgrad Med J 2002;
78:3667.
138. SchlegelL,LemerleS, GeslinP.Lactobacillusspecies asopportunistic
pathogens in immune-compromised patients. Eur J Clin Microbiol
Infect Dis 1998;17:8878.
139. Bayer AS, Chow AW, Betts D, Guze LB. Lactobacillemiareport of
nine cases. Important clinical and therapeutic considerations. Am J
Med 1978;64:80813.
140. Horwitch CA, Furseth HA, Larson AM, Jones TL, Olliffe JF, Spach
DH.Lactobacillemiain three patientswithAIDS.ClinInfect Dis 1995;
21:14602.
141. HusniRN,GordonSM,Washington JA,LongworthDL.Lactobacillus
bacteremia and endocarditis: reviewof 45 cases. Clin Infect Dis 1997;
25:104855.
142. Mackay AD, Taylor MB, Kibbler CC, Hamilton-Miller JMT. Lacto-
bacillus endocarditis caused by a probiotic organism. Clin Microbiol
Infect 1999;5:2902.
143. Presterl E, Kneifel W, Mayer HK, Zehetgruber M, Makristathis A,
Graninger W. Endocarditis by Lactobacillus rhamnosus due to yogurt
ingestion? Scand J Infect Dis 2001;33:7104.
144. Avlami A, Kordossis T, Vrizidis N, Sipsas NV. Lactobacillus rham-
nosusendocarditiscomplicatingcolonoscopy.JInfect2001;42:2835.
256 ADOLFSSON ET AL
by guest on June 6, 2011www.ajcn.orgDownloaded from
... Excessive dietary intake, high accumulation of lipids in hepatic cells as well as increased biogenesis of lipids in lipid droplets and several diet-related difficulties including metabolic syndrome and cardiovascular disease contribute to a condition called nonalcoholic fatty liver disease (NAFLD) (Adolfsson, Meydani, and Russell 2004). The major lipid components are non-polar lipids such as TAG and CEs that is stored in a dynamic organelle known as lipid droplets (LDs) in hepatocytes and in other cells including hepatic stellate cells (HSCs) and Kupffer cells. ...
... However, pro-inflammatory cytokines, oxidative stress, and aberrant hepatic lipid regulation all trigger the deposition of fat in liver tissues and cells like hepatic cells that is hepatocytes and primarily in HSCs. A number of research works pertaining to NAFLD relied on a combination of dietary carbohydrates and fats gathered from various sources, including organic ones (Park et al. 2010;Adolfsson, Meydani, and Russell 2004). Additionally, oxidative stress, which is correlated with obesity, is capable of causing numerous adverse effects such as nephropathy, microvascular difficulties, NAFLD, and endothelial dysfunction (Savini et al. 2013;Kaur 2014). ...
... Dairy products such as yogurt are produced when bacteria like Lactobacillus bulgaricus as well as other lactic acid bacteria (LAB) ferment the lactic acid in milk. It is widely acknowledged to be a high-probiotic meal (Adolfsson, Meydani, and Russell 2004). Living bacteria identified as probiotics have favorable physiological impacts on their hosts. ...
Article
Full-text available
Hepatic steatosis/non‐alcoholic fatty liver disease is a major public health delinquent caused by the excess deposition of lipid into lipid droplets (LDs) as well as metabolic dysregulation. Hepatic cells buildup with more fat molecules when a person takes high fat diet that is excessive than the body can handle. At present, millions of people in the world are affected by this problem. So, it is very important to know the effects of factors responsible for the disease. Here, the role of lipid droplet (LD) biogenesis and metabolism was analyzed and intended to investigate if defects in biogenesis/metabolic enzymes are responsible for the accumulation of lipids other than LDs in fatty liver disease in high‐fat‐induced conditions in mice model. To explore it, high‐fat diet (HFD), fast food (FF), and soft drinks (SD) were administered to wild‐type Swiss albino mice for 14 weeks following yogurt supplementation. After experimental period, glucose tolerance, enzyme function, lipid profile, plasma biochemistry, and other analytical tests were analyzed by auto‐analyzer including different oxidative stress markers. Lipids from hepatic tissues were extracted, and purified by Floatation Assay and subsequently analyzed by different biochemical and chromatographic techniques. Histological architecture of hepatocytes was performed using Zeiss microscope. Finally, increased amount of lipids biogenesis/accumulation was found in liver tissues that causes Fatty liver disease. Significantly, HFD, FF, and SD were identified as factors for the increased LD biogenesis and or lipid metabolic disorder. Nevertheless, yogurt supplementation can homeostasis those LD formation and metabolic syndrome as it increases the down regulation of lipid biogenesis as well as lipid metabolic rate. So, yogurt supplementation was considered as a novel agent for decreasing LD biogenesis as well as excessive accumulation of fat in hepatocytes which can be used as therapeutics for the treatment of NAFLD.
... Additionally, the formation of lactic acid induces the aggregation of milk proteins, giving the yoghurt a distinct gel-like appearance (Nagaoka 2019). Furthermore, earlier reports indicate that yoghurt has numerous health benefits, including the ability to reduce the risk of the common cold, enhance the body immune function (Hemmi et al. 2023), stabilize the intestinal microbiota, and alleviate gastrointestinal disorders (Adolfsson, Meydani, and Russell 2004). Yoghurt has also been shown to reduce the risk of cardiovascular disease by lowering blood cholesterol (Savaiano and Hutkins 2021) and regulating blood pressure (Buendia et al. 2018). ...
Article
Full-text available
Yoghurt is a popular nutrient‐rich food consumed worldwide. It is a functional food, and thus, has many health benefits. As a consequence, its consumer‐market is gradually expanding. However, the production of yoghurt is associated with several problems such as post‐acidification, heat treatment, flavor, cost and technical barriers. To overcome such challenges, various fortification approaches such as the addition of probiotics and prebiotics (as biofortification methods), additives and nutrients (as chemical fortification methods) have been applied. Besides, ultrasound‐assisted or high‐pressure homogenization‐assisted fermentation have been utilized to improve the rheological, textural, flavor and nutritional attributes of yoghurt. This review summarizes the current production processes of yoghurt and their shortcomings, with an emphasis on innovative fermentation fortification techniques.
... 원성 세균들의 발육을 억제하고, 칼슘흡수율도 높으며, 발효시키는 동안 유산균들이 유단백질을 부분적으로 펩 타이드와 아미노산으로 분해하기 때문에 장내 소화율을 높인다 (Chandan et al., 2013). 발효유는 우유 성분 외에 유 산균에 의해 생성된 유기산, 아미노산, 펩티드, 유산균 균체 등 식품으로 영양 (Gilliland, 1990;Sánchez-Segarra et al., 2000)뿐만 아니라, 장내 유해 세균의 억제 및 유용균의 증진 (Adolfsson et al., 2004), 면역계의 자극에 의한 항암 작용 (Meydani and Ha, 2000;Isolauri et al., 2001), 혈중 콜레스테롤의 저하 효과 (Jassim et al., 2020)등 현대인의 성인병 예 방과 건강 증진에 탁월한 기능을 나타내는 것으로 보고되고 있다. 요구르트 제조에 천연식재료를 첨가한 연구는 오디 첨가요구르트 (Kim et al., 2003), 쌀의 저장이 쌀 첨가요구르트에 미치는 영향 (Paik and Ko, 1992), 돼지감자 첨 가요구르트 (Park et al., 2019). ...
... yogurt, calcium would be converted to its ionic form, making it highly bioavailable for intestinal absorption. Additionally, the inhibitory effect of dietary phytic acid on calcium bioavailability would be reduced by the low pH value of yogurt [26]. The low pH value of yogurts also inhibits the growth of pathogens present in the yogurts [27]. ...
Article
Full-text available
INTRODUCTION: Yogurt is a widespread fermented dairy product that offers substantial nutritional and probioticbenefits; though, there is an expanding demand for functional enhancements.OBJECTIVE: This research investigates the impact of inulin, a fructo-oligosaccharide, on enhancing the chemical, mi-crobial, and sensory attributes of yogurt, aiming at improving its overall quality and shelf-life.METHODS: Through a controlled experimental setup, yogurt samples were prepared with 1.5 % concentrations of inulinand analyzed against control samples over different storage conditions.RESULTS: Our findings indicate that the control group has a better sensory profile than the inulin-treated samples andmicrobial stability by fostering the growth of beneficial lactic acid bacteria, thereby enriching the yogurt's probioticprofile. Additionally, sensory evaluations reveal that inulin addition maintains desirable yogurt characteristics,enhancing taste and texture and potentially extending shelf life. These enhancements not only contribute to the prod-uct's nutritional value but also its appeal to health-conscious consumers.CONCLUSION: The study underscores the importance of prebiotics in developing functional dairy products and sug-gests further research to optimize inulin concentrations and explore its synergistic effects with probiotics. Our resultspave the way for the dairy industry to produce high-quality, functional yogurts that cater to the growing demand forhealth-oriented food products.
... A specific portion of lactose consumed at one time may produce significant clinical symptoms while spreading it over several meals, and especially consumed in the company of other products, may lead to leveling or even disappearance of clinical symptoms. The degree of lactose tolerance also depends on the rate of gastric emptying and passage time through the small intestine [80]. ...
Article
Full-text available
Background/Objectives: There is scattered information in the scientific literature regarding the characterization of probiotic bacteria found in fermented milk beverages and the beneficial effects of probiotic bacteria on human health. Our objective was to gather the available information on the use of probiotic bacteria in the prevention of civilization diseases, with a special focus on the prevention of obesity, diabetes, and cancer. Methods: We carried out a literature review including the following keywords, either individually or collectively: lactic acid bacteria; probiotic bacteria; obesity; lactose intolerance; diabetes; cancer protection; civilization diseases; intestinal microbiota; intestinal pathogens. Results: This review summarizes the current state of knowledge on the use of probiotic bacteria in the prevention of civilization diseases. Probiotic bacteria are a set of living microorganisms that, when administered in adequate amounts, exert a beneficial effect on the health of the host and allow for the renewal of the correct quantitative and qualitative composition of the microbiota. Probiotic bacteria favorably modify the composition of the intestinal microbiota, inhibit the development of intestinal pathogens, prevent constipation, strengthen the immune system, and reduce symptoms of lactose intolerance. As fermented milk beverages are an excellent source of probiotic bacteria, their regular consumption can be a strong point in the prevention of various types of civilization diseases. Conclusions: The presence of lactic acid bacteria, including probiotic bacteria in fermented milk beverages, reduces the incidence of obesity and diabetes and serves as a tool in the prevention of cancer diseases.
Article
Full-text available
382 ‫فً‬ ‫وانمستورد‬ ‫محهٍا‬ ‫انمصىع‬ ‫نهٍوغرث‬ ‫انمٍكروبً‬ ‫انتمٍٍم‬ ‫أسواق‬ ‫انبصرة‬ ‫حسه‬ ‫عهً‬ ‫عبذ‬ ‫زٌىب‬ ‫و‬ ‫غضبان‬ ‫كاظم‬ ‫امال‬ ‫اٌجصشح‬ ‫عبِمخ‬ ‫اٌضسالخ،‬ ‫وٍ١خ‬ ‫االغز٠خ،‬ ‫لٍَٛ‬ ‫لسُ‬ ‫انخالصت.‬ ‫عّمذ‬ 26 (‫اٌ١ٛغشد‬ ِٓ ‫ل١ٕخ‬ 13 ‫اٌّصٕك‬ ‫اٌّحٍٟ‬ ‫اٌ١ٛغشد‬ ِٓ ‫ٚل١ٕزبْ‬ ‫اٌّسزٛسد‬ ‫اٌ١ٛغشد‬ ِٓ ‫)ل١ٕخ‬ ‫اٌّمبِ‬ ‫ثٛاسؽخ‬ ٚ ً (11) ‫اٌص١ف‬ ‫ٌّٛسّٟ‬ ‫اٌجصشح‬ ‫ِذ٠ٕخ‬ ‫فٟ‬ ‫اٌّحٍ١خ‬ ‫االسٛاق‬ ِٓ ‫ِٕضٌ١ب‬ ‫اٌّصٕك‬ ‫اٌ١ٛغشد‬ ِٓ ‫ل١ٕخ‬ ٚ ‫اٌىٍ١خ‬ ‫اٌمٌْٛٛ‬ ‫ثىزش٠ب‬ ِٓ ‫وً‬ ‫الذاد‬ ‫لذسد‬ ‫ح١ش‬ ‫ِب٠ىشٚث١ٌٛٛع١ب‬ ‫رحٍ١ٍٙب‬ ‫ٚرُ‬ ‫ٚاٌشزبء‬ E.coli ٚ Salmonella ٚ Staphylococcus aureus ‫ٌٍجش‬ ‫اٌّحٍٍخ‬ ‫ٚاٌجىزش٠ب‬ ‫ٌٍذ٘ٓ‬ ‫اٌّحٍٍخ‬ ‫ٚاٌجىزش٠ب‬ ‫،ث١ٕذ‬ ‫ٚااللفبْ‬ ‫اٌخّبئش‬ ‫ٚالذاد‬ ‫ٚر١ٓ‬ ‫اٌ١ٛغشد‬ ‫ِك‬ ‫ِمبسٔخ‬ ‫الٍٝ‬ ‫ثّسزٜٛ‬ ‫وبٔذ‬ ‫اٌص١ف‬ ‫ِٛسُ‬ ‫فٟ‬ ‫ِٕضٌ١ب‬ ‫اٌّصٕك‬ ‫ٌٍ١ٛغشد‬ ‫اٌجىز١ش٠خ‬ ‫االلذاد‬ ‫اْ‬ ‫إٌزبئظ‬ ‫ٚعٛد‬ ‫ٚ٠الحؿ‬ ‫اٌّٛسّ١ٓ‬ ‫ٌىال‬ ‫اٌّسزٛسد‬ ‫اٌ١ٛغشد‬ ‫لٍٝ‬ ‫اٌّمبًِ‬ ‫فٟ‬ ‫اٌّصٕك‬ ‫اٌّحٍٟ‬ ‫اٌ١ٛغشد‬ ‫رفٛق‬ ‫ِك‬ ‫اٌّسزٛسد‬ ٚ ‫اٌمٌْٛٛ‬ ‫ثىزش٠ب‬ E.coli ‫ِٛسُ‬ ‫خالي‬ ‫إٌّبصي‬ ‫فٟ‬ ‫اٌّصٕك‬ ‫اٌّحٍٟ‬ ‫اٌ١ٛغشد‬ ‫ل١ٕبد‬ ‫عّ١ك‬ ‫فٟ‬ ‫ٚااللفبْ‬ ‫ٚاٌخّبئش‬ ‫ِٕضٌ١ب‬ ‫اٌّصٕك‬ ‫اٌّحٍٟ‬ ‫اٌ١ٛغشد‬ ‫ل١ٕبد‬ ‫ثمط‬ ‫ِبلذا‬ ‫اٌسبٌّٛٔ١ال‬ ‫ثىزش٠ب‬ ِٓ ‫اٌم١ٕبد‬ ‫عّ١ك‬ ‫خٍٛ‬ ‫٠الحؿ‬ ‫،وّب‬ ‫اٌص١ف‬ ‫اٌص١ف.‬ ‫ِٛسُ‬ ‫خالي‬ ‫مفتاحٍت‬ ‫كهماث‬ ‫اٌّ١ىشٚثٟ.‬ ‫اٌزٍٛس‬ ‫اٌّزخّشح،‬ ‫االٌجبْ‬ ، ‫اٌ١ٛغشد‬ : ‫ّمــــت‬ ‫انممذ‬ ‫ه‬ ‫و‬ ‫وو‬ ‫اٌالوز١‬ ‫وبِط‬ ‫حوو‬ ‫ثووبد‬ ‫وً‬ ‫ثفموو‬ ‫زٛص‬ ‫و‬ ‫وو‬ ‫اٌالو‬ ‫سووىش‬ ‫ش‬ ‫و‬ ‫وو‬ ‫رخّ‬ ‫ٔز١غووخ‬ ‫وش‬ ‫ِزخّوو‬ ‫وٟ‬ ‫ٌجٕوو‬ ‫ِٕزووٛط‬ ‫وٛ‬ ‫٘وو‬ ‫اٌ١ووٛغشد‬ ‫ثىزش٠وب‬ ‫ِوٓ‬ ْٛ ‫و‬ ‫اٌّزى‬ Lactobacillus bulgaricus ٚ Streptococcus thermophilus , ‫اٌجٍوذاْ‬ ‫ثموط‬ ‫ٚفوٟ‬ ‫ِضً‬ ‫ش١ٛلب‬ ‫االلً‬ ‫اٌّغٙش٠خ‬ ‫االح١بء‬ ‫رسزمًّ‬ L.lactis ٚ L.helviticus ‫ٚاٌزٟ‬ ‫اٌجبد‬ ‫ِك‬ ‫رخٍػ‬ 1) .) ٚ ‫٠مذ‬ ‫اٌجوشٚر١ٓ‬ ‫ِوٓ‬ ً ‫ِّزبصا‬ ً ‫ِصذسا‬ ‫اٌ١ٛغشد‬ ‫(ف١زوبِ١ٓ‬ ‫ٚاٌشا٠جوٛفالف١ٓ‬ ‫ٚاٌفسوفٛس‬ ‫ٚاٌىبٌسو١َٛ‬ B 2) (‫ٚاٌض١وبِ١ٓ‬ ‫ف١زوبِ١ٓ‬ B 1) ‫وبِ١ٓ‬ ‫ٚف١زو‬ B 12 ، ً ‫وب‬ ‫ل١ّو‬ ً ‫وذسا‬ ‫ِٚصو‬ ‫وه‬ ‫اٌفٌٛ١و‬ ‫وبِط‬ ‫ٌحو‬ ‫وه‬ ‫ٚاٌضٔو‬ ‫و١َٛ‬ ‫ٚاٌّيٕ١سو‬ ‫و١ٓ‬ ‫ٚإٌ١بسو‬ ‫وشٚر١ٓ‬ ‫اٌجو‬ ‫اْ‬ ‫ار‬ ، ‫وبد‬ ‫ٚاٌف١زبِ١ٕو‬ ‫ٚا‬ ‫اٌّزٛاعذح‬ ‫ٌّمبدْ‬ ‫ِوٓ‬ ً ‫ٚاسومخ‬ ً ‫ِغّٛلوخ‬ ‫اٌذسوُ‬ ‫لٍ١وً‬ ‫اٌ١وٛغشد‬ ‫ٚ٠ٛفش‬ ‫لبٌ١خ‬ ً ‫ث١ٌٛٛع١خ‬ ً ‫ل١ّخ‬ ‫ّش‬ ‫رٛف‬ ‫االٌجبْ‬ ‫ِٕزغبد‬ ‫فٟ‬ ِٓ ‫لبي‬ ‫ِحزٜٛ‬ ‫راد‬ ‫ّبد‬ ‫اٌّيز٠‬ ‫ثألً‬ ‫اٌؽبلخ‬. ‫خ‬ ‫و‬ ‫ف‬ ١ ‫ض‬ ‫ى‬ ٌ ‫ا‬ ‫د‬ ‫ب‬ ّ ٠ ‫ز‬ ‫و‬ ‫ي‬ ّ ٌ ‫ا‬ ‫د‬ ‫ا‬ ‫ر‬ ‫خ‬ ‫و‬ ٠ ‫ز‬ ‫غ‬ ‫ال‬ ‫ا‬ ٓ ‫و‬ ِ ٗ ‫و‬ ٍ ‫م‬ ‫ع‬ ‫ب‬ ‫و‬ ّ ِ ، ْ ٛ ٘ ‫ذ‬ ‫و‬ ٌ ‫ا‬ ٓ ِ ٜ ٛ ‫ز‬ ‫س‬ ِ ‫ٚاْ‬ ‫رٕبٚي‬ ٛٔ ‫رحس١ٓ‬ ‫فٟ‬ ‫٠سبلذ‬ ‫وبٌ١ٛغشد‬ ‫االٌجبْ‬ ‫ِٕزغبد‬ ‫اٌيزائٟ‬ ‫إٌفبَ‬ ‫ل١خ‬ ِٓ ‫ٚ٠ض٠ذ‬ ‫اٌيزائ١وخ‬ ‫اٌزٛص١بد‬ ‫رحم١ك‬ ‫فشص‬ (10 ‫٠مٛد‬ .) ‫وبالٌجبْ‬ ‫اٌّزخّش‬ ‫اٌحٍ١ت‬ ‫ِٕزغبد‬ ‫اسزٙالن‬ ‫اٌٝ‬ ‫ٚاالعجبْ‬ ‫ٌجىزش٠وب‬ ‫اٌصوح١خ‬ ‫اٌفٛائوذ‬ ‫ثسوجت‬ ‫اٌحعوبسح‬ ‫فغوش‬ ‫ِضً‬ ‫اٌالوز١ه‬ ‫حبِط‬ Lactobacillus ٚ Bifidobacterium ٚ S.thermophilus (16) ‫اٌج‬ ‫لٍٝ‬ ‫اٌ١ٛغشد‬ ‫٠حزٛٞ‬ (‫ثبٌجشٚثب٠ٛره‬ ‫اٌّمشٚفخ‬ ‫اٌمالع١خ‬ ‫ىزش٠ب‬ Probiotic ‫ثىزش٠ب‬ ‫ِضً‬) Lactobacilli ‫٠موذ‬ ‫ٌوزا‬ ‫أفعً‬ ‫ِٕٙب‬ ‫اٌحذ‬ ‫اٚ‬ ‫ِمبٌغزٙب‬ ‫لٍٝ‬ ‫٠مًّ‬ ‫اٌزٟ‬ ‫اٌصح١خ‬ ‫اٌحبالد‬ ِٓ ‫ثبٌمذ٠ذ‬ ‫السرجبؼٗ‬ ‫ٚـ١فٟ‬ ‫غزاء‬ (13). ‫ِٕزغبد‬ ‫اسزٙالن‬ ‫اسرجػ‬ ‫األٌجبْ‬ ‫ظويػ‬ ‫ٚاسرفبق‬ ‫اٌمفبَ‬ ‫٘شبشخ‬ ‫ٌّشض‬ ‫اٌزمشض‬ ‫ِخبؼش‬ ‫أخفبض‬ ‫ِك‬ ‫ٚسوشؼبْ‬ ‫اٌوذَ‬ ‫اٌذَ‬ ‫فٟ‬ ‫اٌىٌٛسزشٚي‬ ‫ٚاسرفبق‬ ‫اٌمٌْٛٛ‬ ‫ٚاإلسٙبي‬ ِٓ ‫ٚاٌزخف١ف‬ ‫اٌجذأخ‬ ٚ ‫ألشاض‬ (‫اٌالوزٛص‬ ‫سىش‬ ‫رحًّ‬ ‫لذَ‬ 18 .) ‫اٌّزخّش‬ ‫اٌحٍ١ت‬ ‫ِٕزغبد‬ ‫اْ‬ ِٓ ‫اٌشغُ‬ ‫لٍٝ‬ ‫اٌمٕبصوش‬ ‫لٍوٝ‬ ‫ٌٍحفوبؾ‬ ‫ٚسو١ٍخ‬ ‫ِغشد‬ ‫اٌمذَ‬ ‫ِٕز‬ ‫لشفذ‬ ‫لذ‬ ‫اٌ١ٛغشد،‬ ‫ِضً‬ ‫اوزشو‬ ‫لش٠وت‬ ‫ٚلوذ‬ ‫فوٟ‬ ‫أوٗ‬ ‫إال‬ ‫اٌحٍ١ت‬ ‫فٟ‬ ‫اٌيزائ١خ‬ ‫ثسوجت‬ ‫اٌحبصوً‬ ‫اٌزخّوش‬ ‫اْ‬ ‫ف‬ ‫األح١وبء‬ ‫اٌّخزٍفوخ‬ ‫اٌّغٙش٠وخ‬ ‫أدٜ‬ ‫إٌوٝ‬ ‫فوٟ‬ ‫حبٌ١وب‬ ‫رزوٛفش‬ ‫ار‬ ‫اٌّخزٍوف،‬ ‫ٚاٌمٛاَ‬ ‫إٌىٙبد‬ ‫راد‬ ‫إٌّزغبد‬ ِٓ ‫ٚاسمخ‬ ‫ِغّٛلخ‬ ‫رؽٛ٠ش‬ ‫األسوٛاق‬ ‫ِزٕٛلوخ‬ ‫ِغّٛلوخ‬ ‫وبد‬ ‫ِٕزغو‬ ‫ِوٓ‬ ‫وبْ‬ ‫األٌجو‬ ‫وك‬ ‫ٌٚغّ١و‬ ‫وبد‬ ‫ٌٍٛعجو‬ ‫وجخ‬ ‫ِٕبسو‬ ‫األرٚاق‬ ‫و‬ ‫اٚ‬ ‫وُ‬ ‫اٌذسو‬ ‫وً‬ ‫ٚلٍ١و‬ ‫وشا‬ ‫ِزخضو‬ ‫اٚ‬ ‫وبئال‬ ‫سو‬ ‫وٛغشد‬ ‫اٌ١و‬ ‫٠زوٛفش‬ ‫وذ‬ ‫فمو‬ ‫وً‬ ‫بِو‬ ‫ك‬ ‫و‬ ِ ‫د‬ ‫ش‬ ‫غ‬ ٛ ‫و‬ ١ ٌ ‫ا‬ ‫ن‬ ‫ال‬ ٙ ‫ز‬ ‫و‬ ‫س‬ ‫ا‬ ٓ ‫و‬ ‫ى‬ ّ ٠ ٚ ‫خ‬ ١ ‫ل‬ ‫ب‬ ٕ ‫و‬ ‫ص‬ ‫د‬ ‫ب‬ ‫و‬ ٙ ‫ى‬ ٔ ٚ ‫ا‬ ‫ق‬ ‫ب‬ ‫و‬ ٕ ‫م‬ ٕ ٌ ‫ا‬ ٚ ‫ا‬ َ ٛ ‫و‬ ‫ض‬ ٌ ‫ا‬ ً ‫و‬ ‫ض‬ ِ ‫خ‬ ١ ‫م‬ ١ ‫ج‬ ‫ؼ‬ ‫د‬ ‫ب‬ ٙ ‫ى‬ ٔ ‫ا‬ ‫ر‬ ٚ ، ً ‫ب‬ ‫ل‬ ‫ر‬ ‫ال‬ ٚ ‫ا‬ ً ‫ا‬ ٛ ٍ ‫ح‬ ٚ ، ُ ‫س‬ ‫ذ‬ ٌ ‫ا‬ ‫اٌشٛوٛالرٗ‬ ‫أٚ‬ (‫اٌحجٛة‬ 10 .) ‫اٌّىْٛ‬ ‫ِخزٍفخ‬ ‫ح١ٛأبد‬ ِٓ ‫اٌّأخٛر‬ ‫اٌحٍ١ت‬ ‫٠مذ‬ ‫األسبسٟ‬ ‫ِٕزغوبد‬ ‫ِوٓ‬ ‫ٚاسك‬ ‫ٌّذٜ‬ ‫األٌجوبْ‬ ‫٠زّ١وض‬ ‫اٌوزٞ‬ ٚ ‫اٌّزٕٛلوخ،‬ ً ‫غٕ١ب‬ ً ‫ِصذسا‬ ‫ثىٛٔٗ‬ ‫اٌالصِخ‬ ‫االحز١بؼبد‬ ‫رزخز‬ ‫ِبٌُ‬ ‫سش٠مخ‬ ‫ثصٛسح‬ ٚ ‫اٌّ١ىشٚثٟ‬ ٌٍّٕٛ ‫ِضبٌ١خ‬ ‫ث١ئخ‬ ‫رمذ‬ ‫ٚاٌزٟ‬ ‫ثبٌّيز٠بد‬ ٚ ، ‫اٌحٍ١ت‬ ‫رٍٛس‬ ‫اْ‬ ‫ثبألح١بء‬ ‫ثؽش٠مز١ٓ،‬ ‫٠زُ‬ ‫اٌّغٙش٠خ‬ ‫األونى‬ ‫حٍ١وت‬ ‫فوٟ‬ ‫اٌشوبئمخ‬ ‫اٌموذٜٚ‬ ‫٘وٟ‬ : ‫األثموبس‬ ‫ِوشض‬ ‫ثسوجت‬ ‫اٌزٙبة‬ ‫إٌبرظ‬ ‫اٌعشق‬ ‫اٌمٕمٛد٠وبد‬ ‫ِوٓ‬ ‫ِخزٍفوخ‬ ‫أٛاق‬ ِٓ Staphylococci ‫اٌّزسٍسوٍخ‬ ‫اٌّىوٛساد‬ ٚ Streptococci ‫ثجىزش٠ب‬ ‫اٌزٍٛس‬ ‫اٌٝ‬ ‫اظبفخ‬ Escherichia coli ٓ ‫و‬ ِ ٗ ‫و‬ ‫ع‬ ٚ ‫ش‬ ‫خ‬ ‫س‬ ٛ ‫و‬ ‫ف‬ ‫ت‬ ‫و‬ ١ ٍ ‫ح‬ ٌ ‫ا‬ ٟ ‫و‬ ‫ف‬ ‫ب‬ ٘ ‫ذ‬ ‫و‬ ‫ع‬ ‫ا‬ ٛ ‫ر‬ ٟ ‫و‬ ٕ ‫م‬ ٠ ‫ب‬ ‫و‬ ّ ِ ‫ق‬ ‫ش‬ ‫ع‬ ٌ ‫ا‬ ً ‫خ‬ ‫ا‬ ‫د‬ ٟ ‫ف‬ ‫اٌعشق،‬ ‫انثاوٍت‬ ‫اٌزشثخ‬ ‫اٚ‬ ‫اٌٍّٛصخ‬ ‫ٚاالدٚاد‬ ‫ٌالٚأٟ‬ ‫اٌعشق‬ ‫ِالِسخ‬ ‫ثٛسبؼخ‬ ‫اٌعشق‬ ِٓ ‫اٌخبسط‬ ‫اٌحٍ١ت‬ ‫رٍٛس‬ ٟ٘ :
Article
Full-text available
The beneficial impact of gut microbiota on human health has encouraged studies on factors modulating it. Among the different factors, diet plays a vital role in this area. Many studies on animals and humans have been concerned with the effects of fermented milk products on gut microbiota and how they relate to health benefits. Yoghurt, kefir, Koumiss, and fermented kinds of milk made using different probiotic strains were tested for their capability to modulate gut microbiota. It is apparent that the microflora present in fermented milk, specifically probiotics, are capable of enduring the gastrointestinal tract’s adverse conditions primarily through transit microorganisms. Meanwhile, they can alter the gut microbiota in several ways that benefit human health. The present article gives a comprehensive overview of the modulation of gut microbiota by consumption of fermented milk, particularly those containing probiotics, and their impact on human health.
Article
Chokeberry (Aronia melanocarpa) has been traditionally used as a folk remedy due to its health-promoting effects. The aim of this study was to investigate the effects of chokeberry polyphenols combined with the matrices of milk and milk alternatives on the permeability of the intestinal barrier. Based on this, in vitro availability of chokeberry polyphenols was tested by gastrointestinal model combined with a co-culture of human colon adenocarcinoma cells (Caco-2) and human colon cancer cells (HT29-MTX). Additionally, the antioxidant capacity of the samples was analyzed by DPPH (2,2-diphenyl-1-picrylhydrazyl) and ABTS (2,2′-azino-bis(3-ethylbenzothiazoline-6-sulfonic acid) assays. According to the results, both chokeberry juice and chokeberry juice in combination with milk showed a higher recovery of DPPH radical scavenging ability after intestinal digestion. Moreover, a significant difference in the transport of Lucifer Yellow through the intestinal membrane was observed when compared to the control. Therefore, fat- and protein-rich food matrices could represent a potential to increase the bioavailability of phenolic compounds while reducing intestinal barrier injury.
Article
Various fermented milk products are recommended by physicians to restore the lactobacilli in an altered GI-flora. It is, however, not known which fermented milk type is best suited to the purpose or whether lactic starters used by the dairy industry have the ability to survive in gastric juices during digestion in the stomach. Fermented milk types investigated were: 1) buttermilk (filmjolk). containing Streptococcus lactis. Streptococcus cremoris, Streptococcus diace-tylactis, and Leuconostoc citrovorum (cremoris); 2) yogurt containing Lactobacillus bulgaricus and Streptococcus thermophilus; and 3) acidophilus milk containing Lactobacillus acidophilus. In vitro digestion was carried out using a homogenized breakfast mixture consisting of orange juice, cheese sandwich and coffee in amounts supplied in a hospital menu. Human gastric juice (pH = 1.5 to 1.8) was added in proportions normally secreted in the stomach during digestion. The mixture was divided into three samples, to which buttermilk, yogurt or acidophilus milk was added. The pH was noted and a zero time sample was taken immediately, diluted (10⁻³,10⁻⁵,10⁻⁷) and cultivated. The homogenized mixtures with fermented milks added were incubated in a water bath and samples were taken at 1,2, and 3 hr. Samples were cultivated anaerobically at 37 C for 24 hr. The results indicate that the lactobacilli in buttermilk were the first to decrease. After I hr digestion only a few colony forming units were found. The bacteria in yogurt had a higher survival rate than those in buttermilk. However, at the end of the 3rd hr only a few colony forming units were found. The microbes used in acidophilus milk showed the highest survival rate in this investigation; appreciable numbers of colony forming units were found after 3 hr digestion. These results suggest that the microbes of acidophilus milk may pass the stomach barrier in greater number than those of yogurt or buttermilk.
Article
To study the role of food in the stimulation of cytokine production, the effects of lactic bacteria on production of interferon alpha, beta, and gamma; interleukin 1 beta; and tumor necrosis factor alpha were evaluated in mice and humans. Yogurt bacteria induced plasma interferon alpha and beta production in mice. Yogurt intake containing 10(11) bacteria led to increased 2'-5' A synthetase activity in human blood mononuclear cells. This result may suggest an interferon action in a peripheral way. This effect was also found when subjects consumed 10(8) yogurt bacteria/d for 15 d. In an in vitro model, blood mononuclear cells cultured in the presence of yogurt bacteria produced interleukin 1 beta, tumor necrosis factor, and interferon alpha and gamma. These results suggest the involvement of a certain type of food in cytokine production under healthy conditions.
Article
Gastric emptying time and glycemic responses to 400 g regular milk and 400 g ropy milk ('laangfil') were studied in nine healthy non-obese men. One gram of lactose/100 g ropy milk was added to make the lactose content equal in the two milk products. The products were given on two different morning occasions in random order. 99Tc was added to the milk products and gastric emptying recorded by a gamma camera. The emptying time for 50% (t50) of the stomach content was shorter for regular milk (42±10 min) than for ropy milk (62±14 min) (p<0.01). A similar significant difference was found for t75. Regular milk also gave a significantly (p<0.01) larger incremental area under the blood glucose curve (29.4±11.8 mmol x min x l-1) than ropy milk (14.0±12.0 mmol x min x l-1). Ropy milk gave a significantly lower maximal blood glucose and serum insulin peak. The addition of crushed rye crispbread to the two milk products served to three subjects did not change the glucose and insulin response pattern. The low glycemic response to ropy milk compared to regular milk could be explained by its slower gastric emptying rate. This in turn may be due to the higher viscosity of the ropy milk. Although not tested in diabetic subjects, ropy milk may be a good substitute for usual milk in the diabetic diet.
Article
Objectives: We examined whether or not the lactobacilli administered to treat Helicobacter pylori (H. pylori) infection can suppress the colonization of H. pylori, and we also sought to elucidate the mechanism of such suppression. Methods: We used an in vitro culture system and an H. pylori-infected gnotobiotic murine model. Results: Among the lactobacillus species examined in vitro, Lactobacillus salivarius (L. salivarius) but not L. casei or L. acidophilus proved to be capable of producing a high amount of lactic acid and thus completely inhibiting the growth of H. pylori in a mixed culture. The validity of L. salivarius as a probiotic to suppress H. pylori and thus reduce the inflammatory response was again confirmed in vivo by using an H. pylori-infected gnotobiotic murine model. Conclusion: Based on our findings, L. salivarius was found to be a potentially effective probiotic against H. pylori.
Article
A patient is presented with Crohn disease who developed tuberculous pleurisy while treated with azathioprine. The prevalence of opportunistic infections is discussed in patients with inflammatory bowel disease and treated with immunosuppressive regimes.