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Critical Reviews in Food Science and Nutrition
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Evidence for the Effects of Yogurt on Gut Health and
Obesity
Ruisong Peia, Derek A. Martina, Diana M. DiMarcoa & Bradley W. Bollinga
a Department of Nutritional Sciences, University of Connecticut, Storrs, CT.
Accepted author version posted online: 15 Apr 2015.
To cite this article: Ruisong Pei, Derek A. Martin, Diana M. DiMarco & Bradley W. Bolling (2015): Evidence for the Effects of
Yogurt on Gut Health and Obesity, Critical Reviews in Food Science and Nutrition, DOI: 10.1080/10408398.2014.883356
To link to this article: http://dx.doi.org/10.1080/10408398.2014.883356
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Title: Evidence for the effects of yogurt on gut health and obesity.
Authors: Ruisong Pei1, Derek A. Martin1, Diana M. DiMarco1, and Bradley W. Bolling1*
Affiliations: 1Department of Nutritional Sciences, University of Connecticut, 3624 Horsebarn
Rd Extension, Unit 4017, Storrs, CT 06269-4017,
*Corresponding Author (Tel: 860-486-2180; Fax: 860-486-3674; E-mail:
bradley.bolling@uconn.edu)
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Abstract:
Obesity is associated with increased risk for chronic diseases, and affects both developed and
developing nations. Yogurt is a nutrient-dense food that may benefit individuals with lactose
intolerance, constipation and diarrheal diseases, hypertension, cardiovascular diseases, diabetes
and certain types of cancer. Emerging evidence suggests that yogurt consumption might also
improve the health of obese individuals. Obesity is often accompanied by chronic, low-grade
inflammation perpetuated by adipose tissue and the gut. In the gut, obesity-associated
dysregulation of microbiota and impaired gut barrier function may increase endotoxin exposure.
Intestinal barrier function can be compromised by pathogens, inflammatory cytokines,
endocannabinoids, diet, exercise, and gastrointestinal peptides. Yogurt consumption may
improve gut health and reduce chronic inflammation by enhancing innate and adaptive immune
responses, intestinal barrier function, lipid profiles, and by regulating appetite. While this
evidence suggests that yogurt consumption is beneficial for obese individuals, randomized-
controlled trials are needed to further support this hypothesis.
Keywords: yogurt; obesity; inflammation; intestine; chronic disease; bioactives
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INTRODUCTION
Yogurt has been consumed for centuries. As early as 1908, Metchnikoff ascribed the
prolonged life of the Bulgarians to consumption of sour milk fermented by lactic acid bacteria
(O'Sullivan et al., 1992). Yogurt is a milk product fermented by L. bulgaricus, S. thermophilus
and L. acidophilus (CODEX STAN 243-2003). In addition to these Lactic acid bacteria (LAB),
other strains of Lactobacillus and Bifidobacterium are commonly used as yogurt starter cultures
(Desobry-Banon et al., 1999). Yogurts may also be enriched in other probiotic strains that
convey additional health benefits beyond those of traditional yogurt cultures (Shah, 2007).
The global rise in obesity is an increasing health concern. The causes of obesity and
approaches needed to reduce obesity are multifactorial in nature (Holes-Lewis et al., 2013).
Effective social, behavioral, and dietary interventions are needed to mitigate the adverse effects
of obesity on personal health outcomes (Wadden et al., 2012). Obesity impairs gut health, which
may be a potential target for therapeutic dietary interventions (Tilg and Kaser, 2011). Yogurt is
rich with potential bioactive components and emerging evidence points toward the efficacy of
yogurt and its components to improve gut health in obesity.
YOGURT BIOACTIVES
Nutrients
Dairy products are rich in high-quality proteins, calcium, potassium, phosphorus,
magnesium, zinc and B vitamins (Table 1) (Buttriss, 1997). Fermentation can improve the
nutrient content of dairy products. For example, some bacteria synthesize B vitamins. S.
thermophilus can produce folate during yogurt fermentation, and certain inoculations can
increase folate levels 6-fold (Crittenden et al., 2003). Yogurt also contains conjugated linoleic
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acid (CLA), a derivative of linoleic acid (Aneja and Murthi, 1990; Shahani and Chandan, 1979).
CLA may improve body composition by increasing lean body mass while decreasing fat mass,
and has immunostimulatory and anticarcinogenic effects (Park et al., 1997; Whigham et al.,
2000).
Fermentation also improves the digestibility of milk proteins. LAB proteolytic enzymes
and peptidases increase free amino acids in yogurt (Gorbach, 1990). Upon digestion, yogurt had
smaller clots of curd than milk, which facilitated digestive enzyme activity (Breslaw and Kleyn,
1973). In addition, the viscous texture of yogurt might decrease the gastric emptying rate, which
increases duration of the enzymatic hydrolysis (Gaudichon et al., 1994; Shahani and Chandan,
1979).
Yogurt is also considered to be a good source of minerals. Dairy products are a good
source of calcium, not just because of the abundance of calcium but also because of the high
absorbability of calcium from yogurt. The presence of lactose, phosphopeptides, and amino acids
derived from casein in dairy products facilitates the absorption of calcium by promoting its
active transport or passive diffusion (Gueguen and Pointillart, 2000). However, intervention
studies have not demonstrated greater bioavailability of dairy calcium than supplemental calcium
(Recker et al., 1988; Sheikh et al., 1987; Zhao et al., 2005). In contrast, dairy calcium was more
effective than supplementary calcium in reducing weight and fat in energy-restricted adults
(Zemel et al., 2000; Zemel et al., 2004). Although there is no evidence showing that yogurt
serves as a better source of calcium than milk or other dairy products, yogurt has the advantage
of being well tolerated by lactase-deficient individuals (Smith et al., 1985).
Other bioactives
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Dairy products contain bioactive proteins, such as immunoglobulins, α-lactoglobulin, β-
lactoglobulin, lactoferrin, and phosphopeptides, which may regulate immune response, modulate
blood pressure, and facilitate mineral absorption (Ebringer et al., 2008). Bacterial hydrolysis of
milk protein can yield oligopeptides with additional biological activities. For instance, some
peptides (e.g. Val-Pro-Pro and Ile-Pro-Pro) have hypotensive effects via inhibiting angiotensin-
converting-enzyme (Nakamura et al., 2009). A pentapeptide hydrolyzed from casein, Ile-Ile-Ala-
Glu-Lys, has hypocholesterolemic effects in vitro (Morikawa et al., 2007). Other effects of
bioactive peptides such as antithrombotic, antioxidant, antimicrobial and antifungal activities
have also been reported (Ebringer et al., 2008).
Dairy products also contain various bioactive lipids and oligosaccharides. Phospho- and
sphingolipids may reduce blood cholesterol, enhance brain function, and inhibit colon cancer
(Ebringer et al., 2008; Rombaut et al., 2005). Some short chain fatty acids in dairy products such
as butyric acid (C4:0), caprylic acid (C8:0), capric acid (C10:0), lauric acid (C12:0) have
anticarcinogenic, antiviral and antibacterial activities (Ebringer et al., 2008). In addition, dairy
products contain some oligosaccharides such as lactulose, which could serve as prebiotics to
support the growth of commensal bacteria (Marconi et al., 2004).
Microorganisms
S. thermophilus and L. bulgaricus are the most frequent microorganisms used to produce
yogurt. In the United States, some yogurts have additional L. acidophilus, B. bifidum, B. lactis, L.
casei, and/or L. rhamnosus content, among others, and are branded as ‘probiotic yogurts.’ The
most basic definition of probiotics is, “live microorganisms which when administered in
adequate amounts confer a health benefit on the host” (Pineiro and Embarek, 2002). However,
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others have proposed that probiotics must originate from humans, be viable through the
gastrointestinal tract, adhere to the intestinal wall to facilitate colonization, produce
antimicrobials, and provide a demonstrable health effect (Guarner et al., 2005).
It is commonly thought that 105 - 107 CFU/mL living probiotic bacteria are needed to
confer a health benefit to the host (Schillinger, 1999; Vélez et al., 2007). Yogurt culture content
ranges from 104 to 108 CFU/g/strain (Dunlap et al., 2009). In the US, yogurt can be certified with
a “live and active culture” seal from the National Yogurt Association if it contains 108 CFU/g at
the time of manufacture (National-Yogurt-Association, 2008). While the viability of yogurt
microorganisms may be enumerated at manufacture, viability declines throughout the shelf-life
of products. For example, L. acidophilus, a culture commonly added to yogurt post-fermentation,
is relatively unstable in yogurt. This is likely due to hydrogen peroxide produced by L.
bulgaricus during yogurt production (Gilliland and Speck, 1977). A survey of yogurts in
Columbia found poor survival and inconsistent labeling of strains (Vélez et al., 2007). In a study
of yogurts of European origin, bacterial counts in some products were as low as 104 CFU per
gram per strain by the sell-by date (Schillinger, 1999). Temperature fluctuations may also reduce
viability of yogurt probiotics. After 6 h at room temperature, reductions of 9-46.2% were seen in
the CFU count for L. GG, L. johnsonii, and L. acidophilus (Scharl et al., 2010). Thus, it is
expected that the amount of traditional and probiotic strains present in yogurt varies considerably
by manufacturer, storage conditions, and time of consumption. Despite this, yogurt cultures may
not need to be viable to confer a health benefit. For example, a preparation of mixed DNA from
various probiotic strains inhibited colitis in IL-10-/- mice (Jijon et al., 2004). Conventional yogurt
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LAB improve lactose digestion, despite poor viability and the inability to survive the digestive
process (Martini et al., 1991).
OBESITY, YOGURT AND CHRONIC DISEASE RISK
Obesity is an abnormal or excessive accumulation of fat that poses a risk to health. A
person with a body mass index (BMI) between 25 and 30 is classified as overweight and a BMI
greater than 30 is obese. The International Obesity Task Force estimates that at least 1.1 billion
adults are overweight, with 312 million of those obese (Haslam and James, 2005). In the US,
nearly 70% of adults are classified as overweight or obese (Flegal et al., 2010). Obesity is a
major risk factor for a number of chronic diseases such as diabetes, cardiovascular disease
(CVD) and certain cancers. Furthermore, obese adults are projected to lose 7 years of life
expectancy (Peeters et al., 2003). The morbidity associated with obesity accounts for 2-7% of
health care costs in the developed world (Hossain et al., 2007). Morbidities attributed to obesity
include CVD, type 2 diabetes, hypertension, cancer, chronic inflammation, and compromised gut
health. A limited number of yogurt intervention studies relevant to obesity and chronic disease
risk have demonstrated positive outcomes on lipid profiles and chronic inflammation (Table 2).
Cardiovascular disease
CVD is one of the leading causes of death and premature mortality. Ischaemic heart
diseases and stroke account for nearly one in four deaths worldwide (Lozano et al., 2012).
Visceral obesity has a critical role in the development of CVD (Grundy, 2007). Mathieu et al.
reviewed how inflammation linked obesity and CVD (Mathieu et al., 2010). Briefly, excessive
accumulation of fat in the adipose tissue leads to macrophage infiltration and elevated production
of proinflammatory cytokines, which contribute to the development of atherosclerosis. In
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addition, obesity is related to atherogenic dyslipidemia characterized by increased levels of
triglyceride (TG), small dense low-density lipoprotein (sdLDL) particles, as well as decreased
level of high-density lipoprotein cholesterol (HDL-C) (Tenenbaum and Fisman, 2012). Obesity
can also directly affect the structure and functions of the cardiovascular system. Obese
individuals have increased cardiac output which can lead to left ventricular hypertrophy and
other structural abnormalities (Lavie et al., 2009). Obesity also causes left atrial enlargement due
to increased circulating blood volume and abnormal left ventricular diastolic filling (Lavie et al.,
2009). These abnormalities compromise cardiovascular function and increase CVD risk for
obese individuals (Lavie et al., 2009).
Several recent expert reviews have summarized the potential benefits of dairy
consumption on CVD risk. Van Meijl et al. reviewed the physiological effects of dairy
consumption on metabolic syndrome and concluded that dairy calcium and protein had important
roles in reducing metabolic syndrome risk (Van Meijl et al., 2008). In a prospective, matched
case-control study using serum milk fat biomarkers, it was found that biomarkers of milk fat
were inversely associated with the first myocardial infarction in Swedish women after
multivariable adjustment for confounders (OR 0.74, 95% CI: 0.58, 0.94); moreover, reported
intake of fermented milk products were inversely related to the first myocardial infarction (P <
0.05 for trend) (Warensjö et al., 2010). German et al. reviewed the effects of dairy foods and
dairy fats on CVD risk (German et al., 2009). They suggested that although dairy products
contributed to saturated fat intake, there was no consistent association between dairy
consumption and risk of CVD (German et al., 2009). Similarly, another group examined the
influence of milk fat containing dairy foods and CVD health and concluded that dairy
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consumption did not increase the risk of CVD, coronary heart disease or stroke, regardless of
milk fat levels (Huth and Park, 2012). Most research on dairy and CVD risk have not evaluated
yogurt specifically. Given the differences in nutrient and bioactive content between yogurt and
other dairy products, more attention is needed on this specific product category.
Conventional yogurt consumption may improve lipid profiles in healthy and
hypercholesterolemic adults. The effects of conventional yogurt, yogurt with L. acidophilus and
B. lactis, or no yogurt on blood lipids were evaluated in healthy Iranian women (n = 90)
(Sadrzadeh-Yeganeh et al., 2010). Consumption of 300 g/d of conventional and probiotic yogurt
for 6 wk reduced the total cholesterol and total:HDL cholesterol ratio relative to the control
group (Sadrzadeh-Yeganeh et al., 2010). The probiotic yogurt-consuming group also
experienced an 8.8% increase in HDL cholesterol (Sadrzadeh-Yeganeh et al., 2010). Probiotic or
prebiotic containing yogurt may also further improve lipid profiles in adults. A randomized
cross-over study of 40 hypercholesterolemic US adults consuming 200 g yogurt with L.
acidophilus L1 for 4 wk reduced serum cholesterol by 3.2% relative to a yogurt prepared with an
L. acidophilus strain with poor viability and low in vitro cholesterol-lowering activity (Anderson
and Gilliland, 1999). In a cross-over study of 29 healthy women, which included
hypercholesterolemic individuals, 300 g of yogurt with L. acidophilus and B. longum for 7
weeks increased serum HDL cholesterol by 0.3 mmol/L relative to a control yogurt without these
strains (Kießling et al., 2002). In a parallel study of 33 normocholesterolemic women,
consumption of 100 g/d yogurt for 2 wk and 200 g/d for another 2 wk reduced the LDL/HDL
cholesterol ratio in healthy women, with no differences from the probiotic culture L. casei
containing yogurt (Fabian and Elmadfa, 2006). Consumption of 375 mL of yogurt containing L.
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acidophilus and fructo-oligosaccharides for 3 wk lowered serum total cholesterol, LDL-
cholesterol, and the LDL/HDL-ratio in 30 healthy men relative to conventional yogurt
(Schaafsma et al., 1998).
Hypertension
Hypertension is associated with vascular disease mortality, CVD, and renal diseases
(Chobanian et al., 2003; Lewington et al., 2002). Hypertension in US adults increased from
23.9% in 1988-1994 to 29% in 2007-2008 based on data from the National Health and Nutrition
Examination Survey (NHANES) (Egan et al., 2010). Previous studies have indicated a strong
relationship between obesity and hypertension. Cross-sectional studies indicate that more than
85% of hypertensive individuals have a BMI of over 25 kg/m2 (Kastarinen et al., 2000). Several
mechanisms are involved in the pathogenesis of obesity-related hypertension. The sympathetic
nervous system, the renin-angiotensin system (RAS), and aldosterone contribute to the
development of hypertension in obesity (Rahmouni et al., 2005). Long-term over-activation of
sympathetic nervous system which is found in obesity could raise arterial pressure by inducing
peripheral vasoconstriction and increasing sodium reabsorption in the renal tubules (Rahmouni et
al., 2005). Adipose RAS is activated in obesity; animal models of visceral obesity suggest that
adipose RAS contributes to obesity-associated hypertension (Massiéra et al., 2001). Plasma
aldosterone levels were elevated in obese hypertensive patients (Goodfriend and Calhoun, 2004);
on the other hand, an aldosterone antagonist was found to inhibit the development of high blood
pressure in dietary-induced obese dog models (De Paula et al., 2004).
Therefore, given the need for dietary strategies to mitigate hypertension, the
antihypertensive effects of dairy consumption have been investigated. The Dietary Approaches
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to Stop Hypertension (DASH) trial showed that a diet rich in fruits and vegetables lowered blood
pressure and that additional inclusion of low-fat dairy products with reduced saturated and total
fat further augmented these blood pressure-lowering effects (Appel et al., 1997). A recent review
and meta-analysis of five cohort studies involving nearly 45,000 subjects revealed an inverse
association between dairy consumption and development of elevated blood pressure, defined as
≥ 130 mm Hg systolic and/or ≥84 mm Hg diastolic blood pressure (RR 0.87, 0.81-0.94 95% CI)
(Ralston et al., 2012). Another meta-analysis of prospective cohort studies similarly reported that
increased consumption of 200 g/d of low-fat dairy products reduced the risk of hypertension (RR
0.96, 95% CI, 0.93-0.99) (Soedamah-Muthu et al., 2012). Based on these data, low-fat dairy
consumption appears protective against hypertension in adults, but well-designed randomized,
controlled trials (RCTs) are needed to confirm if yogurt is also antihypertensive.
Cancer
In 2010, 8 million people died from cancer globally, accounting for 15.1% of all deaths
worldwide (Lozano et al., 2012). Overweight and obesity are estimated to contribute to 14% of
all cancer deaths in men and 20% of deaths in women (Calle et al., 2003). Meta-analyses indicate
that higher BMI is associated with an increased incidence of endometrial, colorectal, and
postmenopausal breast cancer (Larsson and Wolk, 2007; Moghaddam et al., 2007; Reeves et al.,
2007). It is hypothesized that obesity disturbs the physiological function of adipose tissue, which
leads to insulin resistance, chronic inflammation, and dysregulation of adipokine secretion,
factors contributing to the promotion and progression of cancer (Van Kruijsdijk et al., 2009).
Accumulating evidence indicates potential beneficial effects of yogurt consumption on cancers.
A prospective study involving 82,220 Swedish individuals found that the risk for bladder cancer
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was lowest in individuals consuming the highest levels of sour milk and yogurt (RR 0.62, 95%
CI, 0.46-0.85; ≥ 2 servings/d vs. 0 serving/d) (Larsson et al., 2008). In another prospective study
in an Italian cohort involving 45,241 volunteers, after adjusting for energy, simple sugar,
calcium, fiber, animal fat, alcohol and red meat intake, body mass index, smoking, education,
and physical activity, the hazard ratio for colorectal cancer in the highest versus lowest tertile of
yogurt intake was 0.65 (95% CI, 0.48-0.89) (Pala et al., 2011). Animal studies support the
beneficial effects of yogurt. For example, LABs from yogurt were shown to effectively inhibit
the genotoxic effects of heterocyclic aromatic amines on rats (Zsivkovits et al., 2003). L.
acidophilus isolated from yogurt reduced tumor growth rate and increased lymphocyte
proliferation in a mouse model of breast cancer (Maroof et al., 2012). A potential mechanism for
reduced cancer risk is lower fecal mutagenicity, as demonstrated by consumption of yogurt with
B. lactis by elderly individuals (Matsumoto et al., 2001). Given these promising results for
yogurt intake and reduced risk for bladder and colon cancers, further work is warranted to
evaluate if yogurt is similarly protective against other cancers.
Diabetes
The worldwide prevalence of diabetes in adults was estimated at 6.4% in 2010, and is
projected to increase to 7.7% by 2030 (Shaw et al., 2010). Excess weight may contribute to 90%
of type 2 diabetes cases (Hossain et al., 2007). More than 197 million people worldwide have
impaired glucose tolerance attributed to obesity or metabolic syndrome (Hossain et al., 2007).
Many studies have illustrated the mechanisms linking obesity and type 2 diabetes. Adipose tissue
has a pivotal role in type 2 diabetes by releasing non-esterified fatty acids (NEFAs), hormones,
and various proinflammatory cytokines (Shoelson et al., 2006). Overabundant intracellular
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NEFAs inhibit key enzymes involved in glucose metabolism (Kahn et al., 2006). Furthermore,
the corresponding intracellular fatty acid metabolites activate the serine/threonine kinase cascade
which disturbs the insulin signaling pathway (Shulman, 2000). To compensate for insulin
resistance, the pancreatic β-cells secrete more insulin, eventually causing endoplasmic reticulum
stress and protein misfolding which lead to β-cell apoptosis (Muoio and Newgard, 2008).
Dairy consumption may reduce risk of type 2 diabetes. For example, an 8 yr prospective
cohort study of 82,076 postmenopausal women demonstrated that low-fat dairy products were
inversely associated with the risk of type 2 diabetes (RR 0.65; 95% CI: 0.44-0.96 for the highest
quintile of intake) (Margolis et al., 2011). A recent meta-analysis of cohort studies showed that
the adjusted relative risk of type 2 diabetes for highest versus lowest quartiles of dairy intake was
0.86 (95% CI, 0.79-0.92) (Tong et al., 2011). A subgroup analysis revealed a relative risk of 0.83
(95% CI, 0.74-0.93) for the intake of yogurt (Tong et al., 2011). A newer prospective study
including 340,234 subjects did not find an association between total dairy products and diabetes.
However, in the dairy subtype analysis, a higher combined intake of fermented dairy products
(cheese, yogurt and thick fermented milk) was inversely associated with diabetes (HR, 0.88; 95%
CI, 0.79-0.99) (Sluijs et al., 2012). In another smaller-sized prospective study, fermented dairy
intake was inversely associated with fasting plasma glucose and HbA1c, although no significant
association between intake and incidence of diabetes was found (Sluijs et al., 2012). Although
epidemiological studies support the beneficial effects of yogurt consumption on reduced type 2
diabetes risk, RCTs are needed to confirm the causal effects of dairy consumption on improved
diabetes outcomes.
OBESITY, YOGURT AND CHRONIC INFLAMMATION
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The anti-inflammatory effects of low-fat dairy products have been well documented
(Sakamoto et al., 2001; Schiffrin et al., 2009; Yang and Sheu, 2012). Inflammation is
characterized by redness, swelling, heat, and pain and is typically resolved shortly after the insult
or stimuli are removed (Hotamisligil, 2006). In contrast, obesity-associated chronic inflammation
is unresolved, low-grade inflammation that originates from metabolic cells (e.g. adipocytes) in
response to excessive nutrient intake (Gregor and Hotamisligil, 2011). Overactive metabolic
signals induce the activation of proinflammatory pathways, which cause low-level induction of
cytokines in metabolic tissues; these inflammatory signals recruit immune cells into metabolic
tissues and disrupt the normal metabolic cell functions (Gregor and Hotamisligil, 2011).
Obesity leads to increased levels of inflammatory biomarkers in a variety of tissues
(Table 3). For example, protein kinases such as JNK and inhibitor of κ kinase (IKK) induce the
expression of proinflammatory cytokines (Solinas and Karin, 2010). Obese women had a
significantly higher amount of phosphorylated (active form) JNK in omental fat compared with
lean women (Bashan et al., 2007). In rodents, Hirosumi et al. observed significant increases in
total JNK activity in liver, muscle and adipose tissues of both dietary and genetic (ob/ob) obesity
models (Hirosumi et al., 2002). Increased activation of JNK and NF-κB pathways were also
detected in the hypothalamus of high-fat-fed mice, accompanied by increased secretion of
proinflammatory cytokines (De Souza et al., 2005). Elevated NF-κB and IKK activities were
found in the livers of both genetic and diet-induced obese mice (Cai et al., 2005). In high-fat-fed
mice, increased IKK activity and downstream products of NF-κB pathway were observed in
lysates of the thoracic aorta (Kim et al., 2007). Therefore, the metabolic and inflammatory
consequences of obesity affect a wide variety of tissues. Animal and a limited number of human
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studies indicate a potential role for dairy or yogurt consumption to mitigate chronic inflammation
associated with obesity, as detailed below.
Increased infiltration of immune cells into metabolic tissues
Obesity increases the infiltration of immune cells into various metabolic tissues.
Macrophages infiltrate adipose tissue in obese individuals and are responsible for nearly all
adipose-derived TNF-α expression (Weisberg et al., 2003). Similarly, obesity leads to increased
inflammatory macrophages in visceral adipose tissue (Curat et al., 2006). Macrophage-derived
proinflammatory cytokines can subsequently initiate insulin resistance and compromise β-cells
(Solinas and Karin, 2010).
Animal models of obesity corroborate the infiltration of macrophages and other
immunocytes. Macrophages and microphages were increased in white adipose tissue in both
genetic and high-fat diet-induced models of obese mice (Xu et al., 2003). Ehses et al. observed
increased islet-associated macrophages in high-fat-fed mice and db/db obese mice (Ehses et al.,
2007). Diet-induced obese mice had increased accumulation of T cells in adipose tissue relative
to lean mice (Wu et al., 2007). Likewise, natural killer T (NKT) cells infiltrated visceral adipose
tissue in high-fat-fed mice (Ohmura et al., 2010). In the same model, depletion of NKT cells
ameliorated visceral adipose tissue inflammation (Ohmura et al., 2010).
Yogurt and LAB can modulate the immune response through cytokine production.
However, studies have not focused on the role of yogurt or dairy on obesity-associated
immunocyte dysregulation. In diet-induced obese mice, compared to the high calcium diet, a
nonfat dry milk-supplemented diet reduced weight gain and associated adipose tissue
inflammation as shown by decreased mRNA abundance of (monocyte chemoattractant protein)
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MCP-1, TNF-α, and IL-6; this suggested that some active components in dairy other than
calcium could modulate the immune response (Thomas et al., 2012).
Yogurt and its associated cultures also have immunostimulatory effects in healthy
individuals. Consumption of yogurt containing L. bulgaricus and S. thermophilus increased
production of IFN-γ by T cells in young adults (Halpern et al., 1991). IFN-γ regulates the
induction of pro-inflammatory cytokines and the activation of macrophages and natural killer
cells. LAB directly stimulates human lymphocyte IFN-γ in vitro (De Simone et al., 1986). An
observational retrospective study showed that supplementation with yogurt containing L.
rhamnosus increased the CD4 count in a group of people living with HIV (Irvine et al., 2010).
Consumption of fermented milk containing L. acidophilus significantly increased the
phagocytosis of E. coli in adults (Schiffrin et al., 1997). Likewise, fermented milk with L. casei,
L. acidophilus, or a mixture of both increased phagocytic lymphocytic activities in Swiss mice
(Perdigon et al., 1995). Oral administration of L. acidophilus alone improved immunoreactivity
of peripheral blood leukocytes and peritoneal phagocytes and enhanced serum antibody response
to orally and systemically administrated antigens in mice (Gill et al., 2000). Since yogurt
consumption in obese individuals does not produce pro-inflammatory effects (Labonté et al.,
2013), further work is needed to identify how yogurt modulates immune cells in obesity, and
whether these effects are localized to the gut or have broader activities at metabolic tissues.
OBESITY, YOGURT, AND INTESTINAL BARRIER FUNCTION
The chronic inflammation associated with obesity may be exacerbated by impaired
intestinal barrier function. Leptin-deficient and hyperleptinemic obese mice have increased
intestinal permeability, modified distribution of junction proteins in the intestinal mucosa, as
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well as increased circulating levels of inflammatory cytokines compared with lean control mice
(Brun et al., 2007). Diet-induced obese mice fed high-fat diets had increased intestinal
permeability assessed by gavage of fluorescent-dextran, increased plasma LPS levels, and
reduced expression of genes for tight junction proteins (Cani et al., 2008). Obese women had
increased paracellular permeability measured by lactulose excretion relative to lean women
(Teixeira et al., 2012). Intestinal paracellular permeability was correlated with waist
circumference and HOMA values (Teixeira et al., 2012). Likewise, intestinal barrier function
was more strongly correlated with central adiposity than BMI in overweight adults (Gummesson
et al., 2011). Dysregulation of intestinal barrier function may be attributed to dysregulation of
gut microbiota, endotoxin exposure, the mucus bilayer, secretory immunoglobulin A (sIgA),
antimicrobial peptides, and tight junction proteins. Emerging evidence supports the ability of
yogurt consumption to modulate these functions, as discussed below.
Dysregulation of gut microbiota
The intestine is essential for nutrient absorption and host defense. Gut microbiota
facilitate these functions by fermenting non-digestible nutrients, vitamin synthesis, and
participating in host defense (Salzman et al., 2007). Favorable gut microbiota may compete with
pathogens for space and nutrients and produce anti-microbial compounds such as bacteriocins
and lactic acids (O'Hara and Shanahan, 2006). Gut microbiota also contribute to energy
homeostasis and fat storage. Interestingly, germ-free mice were protected against diet induced
obesity (Bäckhed et al., 2007). On the other hand, conventionalization of germ-free mice with a
normal microbiota harvested from the cecum of conventionally raised mice caused a 60%
increase in body fat within 14 d despite reduced food consumption (Bäckhed et al., 2004). The
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authors proposed that the gut microbiota helped to absorb monosaccharides from the lumen
which further induced de novo hepatic lipogenesis (Bäckhed et al., 2004). Colonization of germ-
free mice with microbiota from obese mice induced a more significant increase in total body fat
than colonization with microbiota from lean mice (Turnbaugh et al., 2006). This suggested that
the composition of gut microbiota affects the development of obesity. In both mice and humans,
Bacteroidetes and Firmicutes are the major species comprising the microbiota (Bäckhed, 2009).
Obese adults have a lower proportion of Bacteroidetes to Firmicutes than lean, although this
ratio can be improved with weight loss from energy restriction (Ley et al., 2006).
Conventional yogurt cultures have limited viability in the gut and a limited ability to
influence the composition of the gut microbiota. Adults consuming yogurt with S. thermophilus
and L. bulgaricus had less than 103 CFU/g of these cultures in feces (Del Campo et al., 2005). In
another study, participants consumed 125 g of a commercial yogurt twice per day for one week,
providing 108 CFU of S. thermophilus and L. bulgaricus (Elli et al., 2006). S. thermophilus was
not present in feces, although L. bulgaricus was present in about 70% of the fecal samples
provided on days 2 and 7 of the yogurt-consumption period. However, the levels of L. bulgaricus
detected on average did not exceed the 105 CFU/g minimum deemed necessary to exert
beneficial effects (Elli et al., 2006). Another study providing a higher dose of yogurt cultures
(375 g yogurt, 108 CFU/g) for two weeks, reported a median value of approximately 104 CFU
each of S. thermophilus and L. bulgaricus per gram of feces (Mater et al., 2005). Although
yogurt cultures have apparently low viability through the entire gastrointestinal tract, more
information is needed about their small intestine viability.
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Certain probiotic strains may have improved viability in the gut relative to S.
thermophilus and L. bulgaricus. Healthy adults that consumed 230 mL yogurt with additional L.
acidophilus and B. bifidum at 107 CFU/g daily for 10 days had decreased aerobic bacteria and
increased anaerobic bacteria in fecal samples (Chen et al., 1999). Additionally, the bifidus to
coliform ratio favorably increased and B. bifidum was measurable for up to 8 days after
consumption (Chen et al., 1999). In contrast, L. acidophilus, S. thermophilus, and L. bulgaricus,
were not detectable in feces (Chen et al., 1999).
McNulty et al (2011) investigated the effect of B. animalis subsp. lactis on the gut
microbiota of mice and humans. Healthy pairs of monozygotic twins consumed a fermented milk
product (FMP) with L. bulgaricus and B. animalis subsp. lactis or no product daily for seven
weeks. Fecal samples analyzed before, during, and after the intervention did not show a
statistically significant change in the microbiota composition (McNulty et al., 2011).
Additionally, the FMP cultures did not persist in the microbiota longer than two weeks after
ceasing its consumption. In the same study, human-gut-derived bacterial strains and FMP strains
were transplanted into germ-free mice. Similar to humans, the humanized intestinal microbiota
was not drastically altered by FMP, but genes related to carbohydrate metabolism were up-
regulated by FMP consumption (McNulty et al., 2011).
Animal models suggest that yogurt-induced improvements in intestinal permeability are
associated with changes to gut microbiota. In Wistar rat pups, consumption of yogurt with L.
casei counteracted acute gastroenteritis-induced barrier dysfunction (Isolauri et al., 1993). In
atopic dermatitis (AD) patients with increased intestinal permeability, 4 wk consumption of
yogurt with B. lactis, L. bulgaricus, and S. thermophilus increased polyamine-producing
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bacterial species which was associated with improved intestinal barrier function (Matsumoto et
al., 2007).
Cultures used in yogurt may also be modified to improve their viability in the gut by
protecting cultures from stomach acid. For example, yogurt with encapsulated or free L.
acidophilus ATCC 4356 was subjected to a simulated human digestive system (Ortakci and Sert,
2012). Encapsulated L. acidophilus had improved viability up to 2 h of incubation in artificial
human gastric juice.
Thus, conventional yogurt cultures have low to no viability in the gut. Probiotic or
encapsulated strains may have greater viability, and their metabolic effects or competition with
coliforms in the intestine are apparent. These studies suggest that strains may not need to adhere
to the intestinal epithelium and proliferate in order to exert the desired health effects. If this is the
case, it suggests that consistent and prolonged probiotic consumption may be needed to achieve
measurable health benefits from these strains.
Contribution of bacterial endotoxin to chronic inflammation
Gut microbiota contribute to systemic low-grade inflammation by increasing the
exposure to proinflammatory bacterial products, especially the Gram-negative-derived LPS
among others (Okamura et al., 2001; Rallabhandi et al., 2006). LPS typically consists of a
hydrophobic domain known as lipid A, a non-repeating core oligosaccharide, and a distal
polysaccharide (Raetz and Whitfield, 2002). LPS initiates inflammatory signaling through LPS
binding protein (LBP), CD14, Toll-like receptor-4 (TLR-4) and MD-2. LBP is thought to extract
LPS and subsequently deliver it to CD14 or lipoprotein; the former may lead to the activation of
target cells while the latter may result in the clearance by liver (Van Bossuyt et al., 1988). CD14
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serves as a pattern-recognition receptor in proinflammatory signaling which can be stimulated by
various ligands (Park et al., 2009; Pugin et al., 1994). MD-2 physically associates with TLR-4 on
the cell surface and acts as co-receptor with TLR-4 for the detection of LPS (Manco et al., 2010).
Once activated by LPS, TLR-4 undergoes oligomerization and recruits its two adaptor protein
pairs, TRAM-TRIF and MAL-MyD88, ultimately activating the NF-κB pathway (Manco et al.,
2010). Human and animal studies have shown LPS as a strong inducer of proinflammatory
cytokines such asIL-6 and TNF in most tissues including adipocytes (Andreasen et al., 2010;
Cani et al., 2007; Creely et al., 2007; Kemna et al., 2005; Stoll et al., 2004).
Overweight and obese adults have increased endotoxin exposure (Sun et al., 2010). Acute
and chronic fat consumption is associated with increased exposure to endotoxin. A cross-
sectional study of 201 healthy French men reported that total energy and fat, but not
carbohydrate or protein were correlated with plasma LPS (Amar et al., 2008). These observations
were confirmed in mice and indicated fat was more efficient in facilitating translocation of LPS
into circulation than carbohydrate (Amar et al., 2008). In addition, a single high-fat meal can
induce postprandial endotoxemia and inflammation (Erridge et al., 2007; Ghanim et al., 2010;
Laugerette et al., 2011). Obesity-associated dysregulation of gut microbiota may also increase
endotoxin exposure (Cani et al., 2007; Cani et al., 2008).
Preliminary studies in elderly individuals have demonstrated that yogurt consumption
inhibits markers of endotoxin exposure in elderly individuals (Schiffrin et al., 2009). Elderly
individuals (n = 23) with small-intestinal bacterial overgrowth consumed 300 g/d of yogurt with
109 CFU L. johnsonii La1 for 4 wk. By the end of the trial, yogurt consumption decreased
plasma levels of LBP and sCD14, LPS pattern recognition receptors in elderly with small-
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intestinal bacterial overgrowth (Schiffrin et al., 2009). Furthermore, yogurt consumption also
reduced plasma endotoxin in healthy elderly participants (Schiffrin et al., 2009). Small intestinal
bacterial overgrowth may affect 41% of obese individuals (Jouet et al., 2011). Therefore, further
studies are warranted to evaluate the ability of yogurt to reduce endotoxin exposure in obese
individuals.
Mucus bilayer
The mucus bilayer is produced by goblet cells and separates gut microbiota from
endothelial cells. This bilayer is formed by a mesh-like structure of mucins, high molecular
weight glycoproteins with increased hydration capacity due to negative surface charges
(Dharmani et al., 2009). Mucins lubricate and maintain the hydrated layer of the epithelium, as
well as create a permeable unstirred, gel-like layer that facilitates nutrient exchange (Dharmani et
al., 2009). The mucus bilayer is essential to the innate host defense. The outer mucus layer
provides space and nutrients for the residence of commensal microflora which might inhibit the
growth and invasion of pathogens; the inner layer is impervious to bacteria and acts like a
protective barrier for the epithelium (Kim and Ho, 2010; Turner, 2009). The goblet cells also
produce intestinal trefoil factor and resistin-like molecule-β, proteins that strengthen the barrier
by stabilizing the mucin polymers or regulating mucin secretions (Dharmani et al., 2009).
Additionally, the mucus layer contains other defensive components such as secretory IgA and
antimicrobial peptides.
Probiotics associated with yogurt may stimulate the production of intestinal mucins and
improve host defense. For example, L. plantarum 299 v incubated with HT-29 intestinal
epithelial cells increased mucin mRNA expression and inhibited the adherence of an attaching
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and effecting pathogenic E. coli. in vitro (Mack et al., 1999). Similarly, in Wistar rats, 7 d
consumption of Lactobacilli, Bifidobacteria, and Streptococci increased basal luminal mucin
content by 60% (Caballero-Franco et al., 2007). Whey peptides derived from α- and β- caseins
also increased mucin secretion in HT29-MTX cells (Martínez-Maqueda et al., 2012). Thus, this
emerging evidence suggests that dairy products or their associated probiotics could be of benefit
to the mucus bilayer. A recent diet-induced obese mice model showed that obesity was
associated with decreased mucus layer thickness due to the decreased level of Akkermansia
muciniphila, a mucus layer resident that played an essential role in mucus turnover (Everard et
al., 2013). Thus, it appears worthwhile to further investigate the effects of yogurt on the obese-
compromised mucus layer.
Secretory IgA (sIgA)
sIgA is the major effector of the mucosa-associated lymphoid tissue (MALT) and
protects against commensal bacterial penetration of the lumen (Brandtzaeg et al., 1999). MALT
consists of lymphocytes such as T cells and B cells, as well as plasma cells and macrophages,
which are stimulated by antigens. sIgA, dimeric or polymeric IgA, is produced by plasma cells in
the intestinal mucosa and is the predominant antibody class in the intestinal lumen (Woof and
Ken, 2006; Macpherson and Uhr, 2004). Interstitial sIgA inhibits pathogens and toxins by 1)
preventing the adhesion and entry of pathogens and toxins by interfering with epithelial receptor
recognition, 2) binding pathogens and promoting their clearance, or 3) inhibiting virus
production (Corthésy, 2007). Low serum IgA may indicate compromised immune function,
while high serum IgA is associated with chronic inflammation, central adiposity, and advanced
age (Gonzalez-Quintela et al., 2008).
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Yogurt consumption appears to modulate the gut immune function by increasing sIgA.
For example, consumption of yogurt with L. acidophilus by 30 healthy adults increased total
serum IgA and the production of specific serum IgA against an attenuated strain of S.
typhimurium (Link-Amster et al., 1994). Consuming 400 mL yogurt with L. acidophilus daily for
4 wk reduced H. pylori and increased the serum IgA level in 38 infected children (Yang and
Sheu, 2012). Rodent studies also support the IgA-promoting effects of yogurt. In a mouse model,
orally administrated LAB alone and in yogurt increased the intestinal IgA producing cells and
IgA (Perdigon et al., 1995). Furthermore, a 7 d yogurt treatment partially prevented the infection
of S. typhimurium and inhibited intestinal carcinomas induced by 1-2-dimethylhydrazine
(Perdigon et al., 1995). Similarly, mice fed yogurt for 4 wk had increased serum IgA after a S.
typhimurium challenge, relative to the milk-treated control group (Puri et al., 1996). Thus, both
animal and human studies have demonstrated induction of sIgA defenses following yogurt
consumption, which may improve immunity.
Antimicrobial peptides
Defensins are antimicrobial peptides secreted by Paneth cells located in the crypts of the
small intestinal mucosa (Porter et al., 2002). Defensins have bactericidal activity against various
Gram-positive and Gram-negative bacteria (Salzman et al., 2007). These peptides facilitate
bacterial membrane collapse through electrostatic and hydrophobic interactions (Zasloff, 2002).
Paneth cell function and defensin levels are compromised in obese individuals, which may be
explained by activated unfolded protein response in the intestine (Hodin et al., 2011). In healthy
women, consumption of 200 mL yogurt with or without B. lactis Bb12 for 3 wk did not alter
fecal β-defensin-2, although both treatments increased fecal sIgA from baseline (Kabeerdoss et
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al., 2011). However, the probiotic Lactobacillus and E.coli Nissle 1917 increased β-defensin 2
expression in Caco-2 cells (Schlee et al., 2008; Schlee et al., 2007). Further work is needed to
determine if dietary approaches are feasible to overcome obesity-compromised defensin
production.
Mucosal cells and tight junctions
The innermost layer of the intestine is a monolayer of enterocytes, endocrine cells,
microfold cells, G cells, and Paneth cells (Scaldaferri et al., 2012). Enterocytes are the most
abundant cells and are connected by apical junctions, which are mainly adherent or tight
junctions (Hartsock and Nelson, 2008). Adherent junctions consist of the transmembrane protein
E-cadherin and the catenin family members, including p120-catenin, β-catenin, and α-catenin
(Hartsock and Nelson, 2008). Adherent junctions initiate and stabilize cell-cell adhesion, regulate
the actin cytoskeleton, and contribute to intracellular signaling (Hartsock and Nelson, 2008).
Tight junctions are composed of occludins, claudins, and junction adhesion molecules (JAM),
transmembrane proteins that are linked to the cytoskeleton through zonula occludens (ZO)
scaffolding proteins (Hartsock and Nelson, 2008). Tight junctions are the primary barrier to
intestinal intercellular space, but are not impermeable. The paracellular pathway is selective to
ions and other small molecules, and depends on the cell type (Tsukita et al., 2001).
Increased plasma endotoxin levels suggest that obese individuals have compromised
intestinal barrier function (Sun et al., 2010). Compromised intestinal barrier function is proposed
to contribute to chronic inflammation in obesity by initiating inflammation through endotoxin
exposure (Cani et al., 2007). The perturbation of proinflammatory cytokines, gastrointestinal
peptides, and endocannabinoids associated with obesity can compromise tight junctions (Bluher
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et al., 2006; Cluny et al., 2012; Côté et al., 2007). In rodents, glucagon-like peptide (GLP)-2
protects barrier function, while melatonin can increase permeability (Cameron and Perdue, 2005;
Cameron et al., 2003; Sommansson et al., 2013). IFN-γ (Bruewer et al., 2005; Clark et al., 2005;
Yang et al., 2002; Youakim and Ahdieh, 1999), TNF-α (Al-Sadi et al., 2009; Li et al., 2008;
Mankertz et al., 2000; Schmitz et al., 1999), and IL-6 (Al-Sadi and Ma, 2007; Yang et al., 2003)
can disrupt barrier function. In contrast, IL-10 (Madsen et al., 1997; Oshima et al., 2001),
transforming growth factor (TGF)-β (Howe et al., 2005), and IL-17 (Kinugasa et al., 2000)
improve barrier function in human T84 colonic epithelial cells. Obese ob/ob mice had improved
barrier function and lower plasma LPS when treated with a CB receptor 1 antagonist (Muccioli
et al., 2010).
Yogurt and its associated probiotics may improve intestinal barrier function by
maintaining the expression of tight junction proteins. Yogurt with B. lactis prevented the
increase in intestinal permeability induced by partial restraint stress in rats, and restored occludin
and JAM-A expression (Agostini et al., 2012). In addition, calcium, which is rich in yogurt,
plays a critical role in tight junction biogenesis and supplementation of calcium was shown to be
able to inhibit alteration in tight junction function in a diabetic rat model (Leal et al., 2010; Stuart
et al., 1994). Therefore, these rodent studies suggest that dairy calcium or probiotic yogurt could
be beneficial for maintaining function of tight junctions.
OTHER POTENTIAL BENEFITS OF YOGURT CONSUMPTION ON GUT HEALTH
Increased yogurt consumption has the potential to improve intestinal health, ameliorate
lactose intolerance, prevent constipation and diarrheal diseases, decrease allergies in vulnerable
populations, and reduce the risks of colon cancer and inflammatory bowel diseases (Adolfsson et
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al., 2004; Parvez et al., 2006). The mechanisms for these actions are not fully described, but may
include modulating gut pH, inhibiting the proliferation and adhesion of pathogenic bacteria,
secreting antibacterial substances, and regulating immune function.
Lactose intolerance
In lactase-deficient individuals, lactose enters the colon and is fermented by colonic
bacteria. The colonic metabolites of lactose include short-chain fatty acids which, together with
electrolytes, introduce an osmotic load that can cause diarrhea and discomfort (Lomer et al.,
2008). In a cross-sectional study, subjects with self-perceived lactose intolerance had a
significantly lower calcium intake from dairy foods and reported higher rate of physician-
diagnosed diabetes and hypertension (Nicklas et al., 2011). Early studies indicated that subjects
with lactase deficiency had better digestion and absorption of lactose from yogurt than the
lactose in milk (Kolars et al., 1984). After ingestion of around 18 g of lactose in water, milk, or
yogurt, subjects receiving yogurt had only one third of the hydrogen excretion, an indicator of
undigested lactose, compared with those receiving lactose in water or milk (Kolars et al., 1984).
Furthermore, the consumption of yogurt led to fewer symptoms of diarrhea and flatulence
relative to milk (Kolars et al., 1984).
Diarrhea
Diarrhea is the leading cause of morbidity and death of children in developing countries
(Boschi-Pinto et al., 2008). Emerging evidence suggests that consumption of yogurt and its
related probiotic cultures prevent or treat diarrhea. In a double-blind, placebo-controlled trial,
infants that received formula with B. bifidum and S. thermophilus reduced the incidence of acute
diarrhea and rotavirus shedding (Saavedra et al., 1994). A meta-analysis of RCTs published from
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1966 to 2000 suggested that Lactobacillus supplementation (108 to 1011 CFU daily) safely
reduced the frequency and duration of acute infectious diarrhea in children (Van Niel et al.,
2002). Moreover, a more recent meta-analysis of RCTs showed that administration of
Lactobacillus through capsules or fermented milk during antibiotic treatment significantly
reduced the risk of developing antibiotic-associated diarrhea (RR 0.35, 0.19-0.67 95% CI) (Kale-
Pradhan et al., 2010). However, the risk reduction was only significant in adults after subgroup
analysis (Kale-Pradhan et al., 2010).
H. pylori infection
Consumption of yogurt with L. gasseri for 8 wk significantly suppressed H. pylori-
induced gastric mucosal inflammation in the elderly (Sakamoto et al., 2001). In children affected
by H. pylori, yogurt consumption decreased serum IL-6 level after 4 wk (Yang and Sheu, 2012).
Inhibition of Colitis
The prevalence of the inflammatory bowel diseases (IBD) Crohn’s disease (CD) and
ulcerative colitis (UC) is increasing in industrialized nations, and although the cause(s) are
unknown, they likely result from an aberrant immune response to intestinal microbiota (Chaves
et al., 2011). Probiotics administered to murine models of IBD improve disease outcomes; this
has been reviewed elsewhere (Claes et al., 2011). Yogurt consumption also inhibits experimental
IBD in mice. Consumption of yogurt with eight L. bulgaricus strains and two S. thermophilus
strains decreased mortality rate and prevented intestinal inflammation and tissue damage in mice
with trinitrobenzene sulfonic acid (TNBS)-induced intestinal inflammation (Chaves et al., 2011).
Yogurt consumption prevented an increase in colonic CD4+ and CD8+ T cell numbers, decreased
TLR-4 positive cells at 14 days, but not 3 or 7 days post TNBS administration (Chaves et al.,
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2011). Yogurt without added probiotic strains inhibited TNBS-induced colitis in mice, increased
the number of IgA producing cells, and decreased CD8+ T cells two wk after TNBS
administration (Gobbato et al., 2008).
Clinical studies have mixed outcomes for the probiotic treatment of IBD and are strain-
dependent (Hedin et al., 2007; Jonkers et al., 2012; Kato et al., 2004; Lorea Baroja et al., 2007;
Miele et al., 2009; Sood et al., 2009). Clinical studies have not used conventional yogurt as an
intervention for IBD, despite self-reported benefits of yogurt reported by IBD patients (Cohen et
al., 2013). Consumption of yogurt with L rhamnosus GR-1 and L. reuteri RC-14 improved
markers of inflammation in monocytes from 20 patients with IBD, including increasing
CD4+CD25 high T cells (Lorea Baroja et al., 2007). Yogurt could be an effective delivery vehicle
for probiotic strains for treatment of IBD. However, more work is needed to identify clinically-
significant probiotic strains for inhibiting colonic inflammation.
Appetite control
Obesity is a result of positive energy balance. Some studies have demonstrated that
yogurt might help reduce energy intake by suppressing appetite. For example, consumption of
yogurt either in semisolid or liquid form led to lower hunger and higher fullness feeling,
compared with a fruit drink or dairy fruit drink (Tsuchiya et al., 2006). Similarly, subjects felt
higher satiety after consumption of yogurt as evidenced by rating of hunger, appetite, desire to
eat, and fullness, compared with ingestion of chocolate bars (Chapelot and Payen, 2010). Yogurt
consumption also suppressed appetite rating and reduced subsequent food intake or delayed
subsequent eating, compared with isovolumetric water (Dougkas et al., 2012; Douglas et al.,
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2013). Therefore, yogurt consumption may provide a further benefit of appetite-suppression,
although the molecular mechanisms for this effect remain uncharacterized.
CONCLUSION
Chronic inflammation is a hallmark of obesity and partially explains the increased risk of
chronic disease in obese individuals. Altered gut microbiota and impaired intestinal barrier
function contribute to the chronic inflammation associated with obesity. Animal models and a
limited number of clinical studies demonstrate that dairy and yogurt consumption reduce chronic
inflammation. New evidence from animal studies indicates that the beneficial effects of yogurt
consumption might also derive from its effects on intestinal barrier function. However, there is
no clinical evidence for the effects of yogurt consumption on inflammation and gut barrier
function in the obese population. The benefits of yogurt for lactose intolerance are well-
established, and emerging evidence supports the ability of yogurt to modulate the gut immunity
and barrier function. Yogurt consumption is beneficial for intestinal health by restoring normal
gut microbiota and suppressing inflammation. Further studies are needed to isolate the effects of
conventional yogurt and yogurt fortified with probiotics, considering that yogurt is a vehicle for
nutrients and other bioactive components. Research investigating the effects of yogurt
consumption on inflammation and intestinal barrier function in the obese population may yield
further insight to the mechanism(s) for its anti-inflammatory effects.
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TABLES
Table 1. Representative nutrient data bank values for plain yogurts in the U.S.A
Nutrient
(per 6 oz) Whole Low-fat Fat-free Fat-free (Greek)
calories 104 107 95 100
total fat (g) 5.9 2.64 0.31 0.66
saturated fat (g) 3.56 1.7 0.12 0.20
MUFA (g) 1.52 0.72 0.05 0.09
PUFA (g) 0.16 0.08 0.01 0.02
cholesterol (mg) 22 10 2 8
carbohydrates (g) 7.92 11.97 13.06 6.12
sugar (g)
B
7.92 11.97 13.06 5.51
dietary fiber (g) 0.0 0.0 0.0 0.0
protein (g) 5.9 6.77 5.73 17.32
thiamin (mg) 0.05 0.08 0.08 0.04
riboflavin (mg) 0.24 0.36 0.40 0.47
niacin (mg) 0.13 0.19 0.21 0.35
vitamin B6 (mg) 0.05 0.08 0.09 0.11
folate (mcg) 12 19 20 12
vitamin B12 (mcg) 0.63 0.95 1.04 1.28
vitamin A (RAE) 46 24 3 2
vitamin C (mg) 0.8 1.4 1.50 0.0
vitamin D (mcg) 3.0 2.0 0.0 0.0
vitamin E (mg) 0.1 0.05 0.0 0.02
vitamin K (mcg) 0.3 0.3 0.30 0.0
calcium (mg) 206 311 338 187
phosphorus (mg) 162 245 267 230
magnesium (mg) 20 29 32 19
sodium (mg) 78 119 131 61
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potassium (mg) 264 398 434 240
iron (mg) 0.08 0.14 0.15 0.12
zinc (mg) 1 1.51 1.65 0.88
A Derived from USDA National Nutrient Database for Standard Reference, Release 26.
BSweetened or fruit yogurts typically have an additional 20 g sugars per 6 oz.
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Table 2. Clinical studies of yogurt on biomarkers relevant to obesity and chronic disease risk.
Category Reference Population Treatment Outcome
Lipid profiles
(Schaafsma et al.,
1998)
n = 30 healthy men
375 mL/d for 3 wk, 0.5%
fat, + L. acidophilus
↓ serum total cholesterol, ↓ LDL, and
↓ LDL/HLD-ratio.
(Anderson and
Gilliland, 1999)
n = 40
hypercholesterolemic
individuals
200 mL/d for 4 wk, + L.
acidophilus, unspecified
fat content
↓ serum cholesterol by 3.2%
(Kießling et al., 2002)
n = 29 women (14
hypercholesterolemic)
300 g/day for 6 mo, 3.5%
fat, + L. acidophilus and
B. longum
↑ HDL
(Fabian and Elmadfa,
2006)
n = 33 lean women
100 g/d for 2 wk and then
200 g/d for another 2 wk,
3.6% fat
↓ LDL/HLD ratio
(Sadrzadeh-Yeganeh
et al., 2010)
n = 90 lean women
300 g/d for 6 wk, 2.5%
fat
↓ total cholesterol and ↓ total:HDL
cholesterol ratio
Inflammation (Matsumoto et al.,
2001)
n = 6 elderly (3 M, 3 F) 100 g/day for 2 wk, + L.
acidophilus and B. lactis,
unspecified fat content
↓ haptoglobin in feces
(Sakamoto et al.,
2001)
n = 31 elderly (29 M, 2
F)
180 g/day for 8 wk, + L.
gasseri, unspecified fat
content
↓ H. pylori-induced gastric mucosal
inflammation
(Schiffrin et al., 2009) n = 36 elderly (9 M, 27 300 g/day for 4 wk, + L. ↓ plasma LBP, sCD14 and surrogate
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F) johnsonii, unspecified fat
content
markers of LPS permeability
(Yang and Sheu,
2012)
n = 38 children 400 mL/day for 4 wk, +
L. acidophilus and B.
lactis, unspecified fat
content
↓ serum IL-6
Appetite (Tsuchiya et al., 2006) n = 32 healthy men and
women
acute yogurt intake (200
Kcal)
↓ hunger, ↑ fullness, ↔ subsequent
food intake
(Chapelot and Payen,
2010)
n = 18 lean men acute yogurt intake (287
Kcal)
↑ satiety, ↔ subsequent food intake
(Dougkas et al., 2012) n = 40 overweight men acute yogurt intake (201
Kcal)
↓ appetite, ↓ subsequent energy intake
(Douglas et al., 2013) n = 15 women acute yogurt intake (160
Kcal)
↓ hunger, ↑ fullness, and delayed
subsequent eating
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Table 3. Obesity-related changes in biomarkers of inflammation.
Reference Samples Population Markers
(Hotamisligil et al.,
1995)
adipose tissue premenopausal
women, n = 18
lean/n = 19 obese
↑ TNF-α mRNA;
body weight reduction ↓ TNF-α
mRNA
(Kern et al., 2001) adipose tissue n = 50 lean/n = 50
obese
↑ TNF-α secretion
plasma ↑ IL-6
(Panagiotakos et al.,
2005)
serum 3042 adults ↑ CRP, ↑ TNF-α, ↑ amyloid A, ↑
IL-6 in subjects with central
adiposity
(Kim et al., 2006) serum 50 obese and 50
lean adults
↑ MCP-1, ↑ IL-8 and ↑ CRP
(Herder et al., 2007)
serum 519 adolescents IL-6, IL-18 and interferon-γ-
inducible protein-10 positively
associated with BMI and waist
circumference
(Mauras et al.,
2010)
plasma 203 children ↑ hsCRP, ↑ fibrinogen, ↑ IL-6 and ↑
plasminogen activator inhibitor-1
(Brake et al., 2006) adipose tissue High-fat-fed male
mice
↑ ICAM-I, ↑ IL-6 and ↑ MCP-1
mRNA
(Ehses et al., 2007) pancreatic
islets
High-fat-fed mice ↑ IL-6, ↑ IL-8 and ↑ macrophage
inflammatory protein 1α
(De Souza et al.,
2005)
hypothalamus High-fat-fed rats ↑ TNF-α, ↑ IL-1β, and ↑ IL-6
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