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KEY WORDS
Yogurt, gut function, gut immunity, gastrointestinal diseases, gut microflora
INTRODUCTION
Am J Clin Nutr 2004;80:24556. Printed in USA. 2004 American Society for Clinical Nutrition
245
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 acidproducing 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.
Am J Clin Nutr
2004;80:24556.
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ADOLFSSON ET AL
B vitamins
Lactose
Lipids
Dairy products and foods prepared with the use of dairy ingredients 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 generally is 6% (3). One example of a significant bacteria-induced
It has been suggested that yogurt and LAB contribute to several facets of gastrointestinal health: the makeup of the gastrointestinal 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 bind to
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 (40 43). 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, and B. 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 intestinal 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 10 18 mo was investigated by GuerinDanan 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. thermophilus and L. bulgaricus were not recovered (43). Bifidobacterium 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).
Another important factor that limits the survival of lactobacilli
within the upper gastrointestinal tract is the inherent ability of the
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 associate with Peyers patches and the lymphoid villous intestinal tissues in mice. Two of the 16 strains investigated, Lactobacillus
acidophilus and L. bulgaricus, are of interest because they relate
to yogurt. It was 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. acidophilus had a low degree of association with Peyers patches
and no association to the lymphoid villous intestinal tissue. Nevertheless, the authors stated that the strains of Lactobacillus
tested showed high rates of survival when Lactobacillus was
administered orally.
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ADOLFSSON ET AL
small intestine of mice in a dose-dependent manner (5). Similarly, a report by Puri et al (56) indicated that S. typhimuriuminduced serum IgA concentrations were significantly higher in
mice fed yogurt over a period of 4 wk than in milk-fed control
mice. This report suggests that the IgA secreted by the challenged
intestinal B cells enters the circulation and increases the concentrations 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
from mice fed yogurt had a higher mitogen-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. acidophilus 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 effects of feeding milk fermented with either L. casei or L. acidophilus 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 production of antibodies to sheep red blood cells. The activation of the
immune system began on day 3, peaked on day 5, and decreased
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
produced by macrophages, T lymphocytes are the source of most
cytokines investigated in those reports. T cells are frequently
classified into 2 categoriestype 1 (Th1) and type 2 (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 Th1 cytokines boost cell-mediated immunity, and the
Th2 cytokines augment humoral immunity. IFN- plays a critical role in the induction of other cytokines and in mediation of
macrophage and natural killer cell activation.
Several reports indicated that consumption of yogurt or intake of
LAB by themselves modulates the production of several cytokines,
such as IL-1, IL-6, IL-10, IL-12, IFN-, and TNF- (60 63).
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 those without LAB (64). Yogurt containing live L. bulgaricus
and S. thermophilus was also reported to augment IFN- 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
types of studies, although feasible with the use of biopsy samples
from the intestines of healthy subjects (65), are difficult to carry
out, and good animal models currently do not exist.
Laxation
Few reports have discussed the effects of yogurt and LAB on
laxation. In the studies published, however, both significant effects (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) of gastric content was significantly greater for ropy milk, an
L. bulgaricus and S. thermophilusfermented milk product
indigenous to Sweden, than for unfermented milk. Another study
showed that milk fermented with L. bulgaricus and S. thermophilus reduced intestinal transit time in human subjects with habitual
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 fermented milk
was consumed. When milk fermented with L. acidophilus was
consumed, the number of defecations increased further to 15/wk.
Studies were conducted of the effects of a commercially available 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 18 45 y (72). Likewise, in a group of elderly
subjects experiencing lengthy orofecal gut transit time but otherwise 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
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ADOLFSSON ET AL
Diarrheal diseases
Diarrhea is a common problem among children worldwide and
has been reported to contribute substantially to pediatric physician visits and hospitalizations in the United States (81). Since
the early 20th century, it has been hypothesized that live bacterial
cultures, such as those used for the fermentation of dairy products, may offer benefits in preventing and treating diarrhea (4).
A recent meta-analysis of randomized, controlled studies by
Van Neil et al (82) found that therapy using Lactobacillus strains
offered a safe and effective means of treating acute infectious
diarrhea in children. Both the duration and frequency of diarrheal
episodes were reduced when compared with those in control
subjects. The benefit of Lactobacillus therapy was seen in diarrheal
diseases caused by various pathogens. The effect of supplementing
formula with B. bifidum and S. thermophilus on preventing the onset
of acute viral diarrhea in infants was examined in a double-blind,
had the most beneficial effect on lactose digestion in these subjects. 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
to environmental factors. For example, it was shown that the lactase
activity of yogurt was preserved and even increased when the yogurt
was subjected to an environment that simulated the temperature
and low pH values of the gut (15). As suggested by the authors, 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.
Pochart et al (76) reported that lactase activity in yogurt decreased by
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 containing 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 fermented milks (50). During the fermentation process, the amount
of lactose present in yogurt is reduced. The lactose content also
varies with the duration of storage after fermentation. In addition,
the bacterial lactase activity corresponds with the survival time of
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
yogurt are recognized as having functional lactase activity and as
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 effect of LAB on
lactose digestion in those suffering from lactose intolerance is
now widely accepted.
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Helicobacter pylori
It has only been 20 y since Helicobacter pylori, a gramnegative, 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 ammoniaproducing 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 produces 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 neutrophils into the gastric wall and local production of IFN-,
proinflammatory cytokines eg, TNF-, IL-1, and IL-6 and
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 documented: H. pylori infection is reported in 90% of duodenal
ulcer patients (119). Treatment of this infection involves the use
of proton 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 viability of H. pylori and less adhesion of the bacteria to human
intestinal mucosal cells after treatment with various Lactobacillus 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,
that preceded the development of colitis. This occurred in parallel 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
oral lactulose therapy, colitis was attenuated. The concentrations
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 patient 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 progression of these diseases is poorly understood. The exact etiology of
IBD is also unknown, but it is likely that, in susceptible persons,
IBD results from an ongoing inflammatory response, which may
be due to a defect in both the regulation of the mucosal proinflammatory response and the function of the intestinal epithelium. Currently, evidence suggests that yogurt and LAB have
modest clinical benefits and are safe for use in patients with these
conditions. Further studies are required to ascertain whether yogurt is beneficial as a prophylactic or a therapeutic regimen for
IBD (or both) and to establish exactly which mechanisms are
involved.
SAFETY
Although the safe use of nonsporing anaerobic LAB in fermented foods is widespread and has a long history, there have
been occasional reports associating LAB with clinical infections
(53, 136) because benign microorganisms have been shown to be
infective when a patient is severely debilitated or immunosuppressed (137, 138). Some of the diseases that have been associated with LAB infection include septicemia, infective endocarditis, 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 immunosuppressive therapy and 23 had received antibiotics. In none of these
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 gastrointestinal tract (142144). However, as with lactobacillemia, no reports to date have been able to identify a connection between
LAB from fermented milk and infection in humans. In most of
these cases, the origin of the Lactobacillus is most likely the host.
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