research studies on yogurt

An official website of the United States government

Official websites use .gov A .gov website belongs to an official government organization in the United States.

Secure .gov websites use HTTPS A lock ( Lock Locked padlock icon ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.

• Publications
• Account settings
• Advanced Search
• Journal List

Yogurt consumption is associated with better diet quality and metabolic profile in American men and women

Huifen wang, kara a livingston, caroline s fox, james b meigs, paul f jacques.

• Author information
• Article notes
• Copyright and License information

Corresponding author. Tel.: +1 617 556 3322; fax: +1 617 556 3344, [email protected]

Issue date 2013 Jan.

The evidence-based Dietary Guidelines for Americans recommends increasing the intake of fat-free or low-fat milk and milk products. However, yogurt, a nutrient-dense milk product, has been understudied. This cross-sectional study examined whether yogurt consumption was associated with better diet quality and metabolic profile among adults (n = 6526) participating in the Framingham Heart Study Offspring (1998-2001) and Third Generation (2002-2005) cohorts. A validated food frequency questionnaire was used to assess dietary intake, and the Dietary Guidelines Adherence Index (DGAI) was used to measure overall diet quality. Standardized clinical examinations and laboratory tests were conducted. Generalized estimating equations examined the associations of yogurt consumption with diet quality and levels of metabolic factors. Approximately 64% of women (vs 41% of men) were yogurt consumers (ie, consumed >0 servings/week). Yogurt consumers had a higher DGAI score (ie, better diet quality) than nonconsumers. Adjusted for demographic and lifestyle factors and DGAI, yogurt consumers, compared with nonconsumers, had higher potassium intakes (difference, 0.12 g/d) and were 47%, 55%, 48%, 38%, and 34% less likely to have inadequate intakes (based on Dietary Reference Intake) of vitamins B2 and B12, calcium, magnesium, and zinc, respectively (all P ≤ .001). In addition, yogurt consumption was associated with lower levels of circulating triglycerides, glucose, and lower systolic blood pressure and insulin resistance (all P < .05). Yogurt is a good source of several micronutrients and may help to improve diet quality and maintain metabolic well-being as part of a healthy, energy-balanced dietary pattern.

Keywords: Yogurt, Milk, Diet, Nutrition status, Metabolic profile, Human

1. Introduction

The Dietary Guidelines Advisory Committee 2010 identified 10 nutrients that were inadequate in the diet of adult American men and women, including vitamins A, C, D, E, and K and choline, calcium, magnesium, potassium, and dietary fiber [ 1 ]. Dairy may play an essential role in helping to meet the recommendations for some of these shortfall nutrients [ 2 ]. An overall higher diet quality has been observed with increased dairy consumption [ 3 - 6 ]. In addition, although evidence has not been consistent, increasing intake of dairy products may be associated with lower risk of cardiovascular disease and type II diabetes [ 7 - 10 ]. In particular, fat-free or low-fat milk and milk products have been recommended by the Dietary Guidelines for Americans (DGA) as one of the food groups for which consumption should be increased [ 11 ]. However, few related epidemiological studies have differentiated between types of dairy products or specifically focused on yogurt.

Yogurt is a dairy product fermented by lactic acid bacteria. Although it generally has a similar micronutrient composition as milk, yogurt is highly concentrated with proteins and vitamins and minerals, such as vitamin B2 and B12, calcium, magnesium, potassium, zinc, and others [ 12 ]. For example, low-fat yogurt contains approximately 50% more potassium, calcium, and magnesium per 8-oz serving than low-fat milk [ 13 ]. Despite limited evidence, yogurt consumption has been inversely linked to weight gain, common carotid artery intima-media thickness, metabolic syndrome, and type II diabetes [ 8 , 14 - 16 ]. Therefore, increasing low-fat yogurt intake may be important for improving the diet quality and health among Americans.

The current study aimed to explore the relation of yogurt consumption with diet quality (focusing on shortfall nutrients) and metabolic profile among the adults involved in the Framingham Heart Study (FHS). We hypothesized that yogurt consumers and greater yogurt consumption would be related to better diet quality and healthier metabolic status independent of better diet quality.

2. Methods and materials

2.1. study population.

The current study used data from the FHS Offspring Cohort and Generation Three Cohort. The detailed information about these 2 cohorts can be found elsewhere [ 17 ]. Briefly, the FHS, which started in 1948, is a longitudinal population-based study of cardiovascular disease. A total of 5124 offspring (aged 5-70 years) of the original FHS cohort were recruited to participate in the FHS Offspring Cohort Study in 1971. As of 2008, 8 examination cycles had been conducted. The Generation Three Cohort, initiated in 2002, included 4095 adults (aged 19-72 years) with at least 1 parent in the FHS Offspring cohort and their spouses. Two examinations have been conducted among the Generation Three Cohort. At each examination, participants underwent a standardized medical history and physical examination. Dietary intake was assessed among the Offspring Cohort, beginning with examination 5, and the Generation Three Cohort. Study protocols and procedures were approved by institutional review boards for human research at Boston University and Tufts Medical Center and the Massachusetts General Hospital. Written informed consent was obtained from all participants.

For the current cross-sectional study, we combined the data from the Offspring Cohort examination 7 (1998-2001, n = 3539) and the Generation Three Cohort examination 1 (2002-2005, n = 4095). Among these 7634 participants, those with missing (n = 709) or invalid (n = 256) food frequency questionnaire (FFQ) data were excluded from analyses. An invalid FFQ was defined as a reported total energy intake of less than 600 kcal/d for all or greater than 4000 kcal/d for women and greater than 4200 kcal/d for men or more than 12 blank food items. The participants with missing data on yogurt consumption (ie, consumption status or percentage of energy contribution from yogurt) (n = 143) were further excluded, leaving 6526 participants (aged 19-89 years) for the analyses. Compared with those who remained in the analyses, participants who were excluded were older and less healthy (data not shown).

2.2. Dietary assessments

Before each examination, a 126-item semiquantitative FFQ [ 18 ] was mailed to every participant. Participants were asked to bring the completed FFQ with them at their FHS examination visit. The relative validity of the FFQ has been reported previously [ 18 - 20 ]. Participants were asked how often, on average, during the past year they consumed a standardized serving size of each food (eg, 1 cup yogurt). There were 9 frequency categories ranging from “never or less than one serving per month” to “more than six servings/d.” Separate questions also assessed the use of vitamin and mineral supplements, types of breakfast cereal and cooking oil, and information about certain cooking and eating behaviors. The daily nutrient values were calculated by multiplying the nutrient content of the specific portion size of each food (based on the Harvard nutrient database) by the daily consumption frequency and summing all related food items. Specifically, for the dietary analysis, yogurt was coded as “yogurt with fruit, low-fat, containing 10g protein per 8oz” in the database [ 18 ]. The detailed information about the nutrient components in yogurt has been documented [ 13 ].

The Dietary Guidelines Adherence Index (DGAI) was created to measure the overall dietary quality according to the adherence of participants to the key dietary recommendations by the 2005 DGA [ 21 ]. Detailed information about the development and application of DGAI can be found elsewhere [ 21 ]. Briefly, a total of 20 index items were included in the calculation of DGAI score, including 11 items (ie, food intake subscore) assessing adherence to energy-specific food intake recommendations and 9 items (ie, healthy choice subscore) assessing adherence to “healthy choice” nutrient intake recommendations. Each item was scored ranging from 0 to 1 based on the degree of the adherence, so the maximum possible DGAI score is 20 indicating a complete adherence. The DGAI penalizes on overconsumption of discretionary energy and energy-dense foods, which is an important feature of DGAI over other a priori–defined index scores [ 21 ].

2.3. Measurements of other variables

All clinical examinations were performed at the NHLBI Framingham Heart Study site in Framingham, Massachusetts. A standardized physical examination was conducted, and questionnaires were used to assess participants' lifestyles (eg, physical activity for a typical day) and medical history. A physical activity index (PAI) score, expressed in metabolic equivalents, was calculated by averaging the number of hours spent on specific activities (ie, sleep, sedentary, slight activity, moderate activity, and heavy activity) and weighting on the oxygen consumption required to perform these activities [ 22 ]. Height (to the nearest 0.25 in) and weight (to the nearest 0.25 lb) were measured with the participant standing, shoes off, and wearing only a hospital gown. Body mass index (BMI) was then calculated in kilograms per square meter. Sitting blood pressure was measured twice on the left arm of each participant after a 5-minute rest using a mercury column sphygmomanometer and a standardized protocol, and 2 readings were averaged for the analyses [ 23 ].

Fasting (≥8 hours) blood samples were drawn and analyzed in the Framingham Heart Study Laboratory (Framingham, MA) for assessing glucose and lipid levels [ 17 ]. A hexokinase/ glucose-6-phosphate dehydrogenase method [ 24 ] was used to measure serum glucose. Plasma total cholesterol and triglycerides were measured by enzymatic methods [ 25 ], and high-density lipoprotein (HDL) cholesterol was measured after dextran-magnesium precipitation [ 26 ]. The intra-assay and interassay coefficients of variation were all less than 2% and less than 3%, respectively, for glucose, triglyceride, total cholesterol, and HDL cholesterol. For the Offspring Cohort, fasting insulin concentrations were measured using radioimmunoassay; the intra-assay coefficient of variation was 3.9%, and the interassay coefficient of variation ranged 4.7% to 6.1% [ 17 ]. For the Generation Three Cohort, fasting insulin concentrations were measured using enzyme-linked immunosorbent assay; the intra-assay and interassay coefficients of variation were 2.7% and 8.1%, respectively [ 17 ]. Fasting insulin values from the Generation Three Cohort were standardized for aggregation with the Offspring cohort to counter the difference in methods [ 17 ]. The homeostasis model assessment of insulin resistance (HOMA-IR) was calculated accordingly: HOMA-IR = (glucose [mg/dL] × insulin [mU/L])/405 [ 27 ].

2.4. Statistical analyses

All analyses were conducted using SAS statistical software (version 9.2; SAS Institute, Cary, NC). Skewed data were log transformed for the analyses and back transformed to present. Generalized estimating equations (GEEs) were used, as appropriate, to control for the family correlation between Offspring and Generation Three Cohorts.

Participants were grouped as yogurt consumers (>0 servings/week) vs nonconsumers (0 servings/week). Consumers were further divided into 2 groups (ie, low-intake group and high-intake group) using the median amount of (ie, energy contribution [%kcal])) their yogurt consumption as the cut point. Mean values or percentage of participants' characteristics and dietary intakes of selected food groups were calculated and compared across yogurt consumption groups.

To assess the prevalence of nutrient (excluding nutrients from supplements) inadequacy among the current study population, the estimated average requirements (EAR) cutoff method [ 28 ] was used. The percentage of the population with usual intakes below the EAR is an appropriate estimate for the prevalence of the group with inadequate intakes, under the assumptions of no correlation between intakes and requirements, greater variance in intakes than in requirements, and the symmetrical distribution of requirements around the EAR [ 28 ]. The prevalence of nutrient inadequacy was compared between yogurt consumers and nonconsumers.

The EAR cutoff method may not be appropriate for iron due to the skewed distribution of the requirements of iron [ 28 ]. In this regard, the probability method [ 29 ] was used for estimating the prevalence of iron inadequacy. In addition, because no EAR was available for the dietary intakes of fiber and potassium, we used the adequate intake (AI) as a reference. Individuals with usual intakes greater than 100% of AI had 0% probability of inadequacy, whereas the prevalence of inadequacy among people whose usual intake of 100% or less of AI could not be estimated [ 28 ].

Generalized estimating equation models with Logit link were used to examine whether yogurt consumption (ie, dichotomized or in 3 groups [nonconsumers, low-intake, and high-intake groups]) was associated with a lower likelihood of being inadequate in nutrient intakes, focusing on the “shortfall” nutrients (ie, high prevalence of inadequacy), except for potassium and fiber. Generalized estimating equation models with Identity link assessed the relations of yogurt consumption with the overall diet quality represented by DGAI score, the intake of potassium and fiber, and metabolic profile (including levels of total cholesterol, HDL cholesterol, triglycerides, glucose, blood pressure, and HOMA-IR). Models were adjusted, as appropriate, for participants' age, sex, smoking status, PAI score, total energy intake, DGAI score, BMI, and the use of corresponding dietary supplements (eg, in the analyses of vitamin B6 inadequacy, we adjusted for the use of multiple vitamins, vitamin B6, or B complex vitamins). For the analyses of metabolic profile, the use of any vitamin and mineral supplement was included as a covariate. In addition, the use of cholesterol-lowering, antidiabetics, or antihypertensive medications was also examined as covariates in the corresponding models. However, the adjustment of these factors did not materially change the results but reduced the sample size due to some missing data on the medication use and thus was not included in the final models. The linear trend across the 3 groups of yogurt consumption was tested by using the median yogurt intake in each group as a continuous variable.

Two sets of sensitivity analyses were conducted. First, we examined the nutrient inadequacy across yogurt consumption groups (ie, consumers vs nonconsumers and nonconsumers vs low-intake group vs high-intake group) using data of total nutrients from foods, supplements, and fortification. Second, all analyses (including first set of sensitivity analyses) described above were repeated while excluding potential outliers of yogurt consumption, that is, the participants whose energy contribution from yogurt was greater than 99th percentile of population distribution.

In addition, we also conducted a cluster analysis to identify the dietary patterns that were associated with yogurt consumption among this FHS population. Generalized estimating equation models were used as appropriate to examine the association between yogurt consumption and the identified dietary patterns among men and women. The details of this cluster analysis are presented as the Supplemental Material

All statistical tests were 2 sided. Statistical significance was set at P < .05.

There were 41.4% of men and 64.2% women consuming yogurt. The average energy contributions of yogurt among men and women were 1.38% and 2.75%, respectively. Participant characteristics are shown in Table 1 . Compared with nonconsumers, yogurt consumers appeared to have better metabolic profile, such as lower BMI, waist circumference, levels of triglycerides, fasting glucose and insulin, and blood pressure but higher HDL cholesterol. Yogurt consumers consumed less percentage of energy from processed meat, refined grains, and beer than nonconsumers. In contrast, the consumption of healthy foods tended to be greater in yogurt consumers vs nonconsumers, such as fruits, vegetables, nuts, fish, and whole grains, and others. This was consistent with our observations in the cluster analysis ( Supplemental Material ) where we found that yogurt consumers were about twice as likely to have a healthier dietary pattern than nonconsumers.

Table 1. Unadjusted participants' characteristics by yogurt consumption groups: Framingham Heart Study Offspring (1998-2001) and Generation Three Cohorts (2002-2005) (n = 6526).

P values for testing the differences between yogurt consumers and nonconsumers (tests were conducted in GEE Models with Identity Link for continuous variables and Logit Link for categorical variables; skewed continuous data were log transformed before entering the tests).

Means ± SD or percentage.

Yogurt consumers had significantly lower prevalence of nutrient inadequacy than nonconsumers ( Table 2 ), and there were more consumers with usual intake of potassium and fiber above AI (all P < .01). After adjusting for age, sex, physical activity, smoking status, BMI, and the use of dietary supplements, yogurt consumption was associated with better overall diet quality as reflected by DGAI score, mean intake of potassium and fiber, or the likelihood of nutrient inadequacy ( Tables 3A and 3B ). However, further controlling for DGAI score, the relations between yogurt consumption and the inadequacy of fiber; folate; and vitamins B1, B6, C, and E were all eliminated. In contrast, yogurt consumers' (vs nonconsumers') potassium intakes remained higher (difference, 0.12 g/d) and were 47%, 55%, 48%, 38%, and 34% less likely to have inadequate intakes of vitamins B2 and B12, calcium, magnesium, and zinc, respectively (all P ≤ .001).

Table 2. Population distribution of nutrient (excluding supplements) intake status among yogurt consumers vs nonconsumers.

P values were all less than .001 for the difference between groups(tests were conducted in GEE Models with Logit Link).

The percentage of population with inadequate nutrient intake for all such values.

Because EAR are not available for potassium and fiber to define nutrient inadequacy.

Table 3. Table 3A The associations of yogurt consumption with diet quality and the intake of potassium and fiber (nutrients excluding supplements).

Low-intake and high-intake groups were generated using a cut point of 2.07%kcal from yogurt.

P values for testing the linear trends across yogurt consumption (percentage of energy contribution) groups.

P values for testing the differences between yogurt consumers and nonconsumers.

Model 1adjusted for age, sex, total energy intake, PAI score, smoking status, BMI, and the use of corresponding dietary supplements (wherever data were available). Model 2 adjusted for covariates in model 1 and DGAI score.

Odds ratio (95% CI) for all such values.

As shown in Table 4 , compared with nonconsumers, yogurt consumers had lower levels of triglycerides (107.0 [95% confidence interval {CI}, 104.2-109.8] vs 111.2 [108.4-114.0] mg/dL), fasting glucose (97.2 [96.5-97.9] vs 98.7 [98.0-99.5] mg/dL), and insulin (81.4 [79.9-82.9] vs 83.8 [82.2-85.4] pmol/L), systolic blood pressure (120.2 [119.5-120.9] vs 121.7 [121.0-122.3] mm Hg), and HOMA-IR score (3.27 [3.20-3.35] vs 3.42 [3.34-3.50]) (all P ≤ .001). Despite being attenuated when further controlled for DGAI score and the use of supplements, these inverse associations remained significant for fasting glucose ( P = .02) and systolic blood pressure ( P = .01). In addition, people with high intake of yogurt had lower levels of triglycerides ( P linear = .02), fasting insulin ( P linear = .02), and HOMA-IR ( P linear = .006) than nonconsumers. However, there was no association between yogurt consumption and levels of total and HDL cholesterol, and accounting for participants' BMI substantially attenuated many of the associations between yogurt consumption and examined metabolic factors.

Table 4. The associations between yogurt consumption and levels of metabolic factors.

Model 1: adjusted for age, sex, PAI score, total energy intake, and smoking status. Model 2: model 1 + DGAI score and the use of supplements. Model 3: model 2 + BMI.

Mean (95% CI) for all such values;

Triglycerides, glucose, insulin, and HOMA-IR are presented in geometric means (95% CI).

The sensitivity analyses generated similar findings as the primary analyses (data not shown).

4. Discussion

Among these 6526 middle-aged to older men and women, as we had hypothesized, yogurt intake was associated with better overall diet quality, greater intakes of several shortfall nutrients, and healthier metabolic profiles independent of overall diet quality.

Yogurt constituted up to 32% of dairy in European diets [ 30 ], whereas it only accounted for 5% or less of total dairy intake among men and women and across different ethnic groups in the United States [ 16 ]. As a dairy source with high concentration of various nutrients [ 13 , 31 ], increasing yogurt consumption among Americans may lead to more nutrient dense diets and greater adequacy for some of the shortfall nutrients, if substituting for energy-dense foods. However, although the health benefits of yogurt have been widely proposed and investigated in animal models, limited epidemiologic evidence is available, and potential mechanisms are unclear [ 15 , 32 ]. Particularly, different from being fed in animal models, yogurt is generally consumed among free-living human populations in the context of other foods and lifestyles. Therefore, for better elucidating the benefits of yogurt, the dietary patterns and diet quality that are associated with yogurt consumption should be taken into account. Among the FHS adult cohorts, yogurt consumers were more likely to follow a healthier dietary pattern that featured a higher intake of other reduced fat dairy, fruits and vegetables, tofu and beans, nuts and seeds, poultry, fish and other seafood, whole grains, and red wine (shown in Supplemental Material ). In concordance, yogurt consumers had significantly higher DGAI score than non-consumers, suggesting that consumers were more likely to have a better overall diet quality by adhering to the key DGA intake recommendations [ 21 ]. Because the healthy foods recommended by DGA, including yogurt, tend to be nutrient dense, it is not surprising that we observed a much lower prevalence of nutrient inadequacy among yogurt consumers than nonconsumers. In this regard, our findings were also consistent with the previous report that the dietary variety of nutrient-dense foods was positively associated with nutrient adequacy [ 6 ].

Yogurt possesses similar, although more concentrated, micronutrient composition to that of milk. However, none of dietary fiber; folate; and vitamins A, D, E, and C was present in notable quantities in the current studied low-fat yogurt [ 13 ]. Therefore, as expected, the associations between yogurt consumption and the adequacy of these nutrients were substantially attenuated after adjusting for the DGAI score. Any of the residual significant associations between yogurt intake and these nutrients may be due to the relatively large study sample size as well as the unmeasured residual confounding that accompanied yogurt consumption.

Based on the amounts of nutrients that are required to meet the EAR and AI [ 33 , 34 ], the low-fat yogurt examined in the current study is an excellent source of calcium, magnesium, potassium, zinc, and vitamins B2 and B12 [ 13 ]. Although the current evidence does not suggest that calcium in yogurt is better absorbed than that in milk [ 35 , 36 ], the simple fact that concentrations of some micronutrients are higher in yogurt would result in greater availability of these nutrients for utilization in the body [ 12 ]. In addition, yogurt may be well tolerated for lactase-deficient individuals [ 35 , 37 ]. Consistently, we observed that, even after controlling for the DGAI score, yogurt consumption remained robustly associated with lower prevalence of inadequacy for these vitamins and minerals and mostly in a dose-response manner.

In the present cross-sectional analyses, yogurt consumption was inversely related to levels of triglycerides, glucose and insulin, insulin resistance, and blood pressure, when adjusting for demographic and lifestyle factors. Our results were in agreement with some previous evidence [ 8 , 14 - 16 ]. One more serving of yogurt per day was linked to less 4-year weight gain (−0.82 lb) among 120000 or more American men and women [ 15 ] and 60% lower prevalence of metabolic syndrome among US adults in the 1999-2004 National Health and Nutrition Examination Survey [ 16 ]. By following a cohort of elderly women for 3 years, Ivey et al [ 14 ] reported that participants who consumed more than 100-g yogurt per day had a significantly lower common carotid artery intima-media thickness than did participants with lower consumption. In addition, a meta-analysis of 4 studies targeting yogurt revealed that yogurt consumption was also associated with lower risk of type II diabetes [ 8 ].

It should be noted that the significant associations between yogurt consumption and metabolic factors that we found were attenuated after further controlling for the DGAI score and the use of supplements. The association between yogurt consumption and diastolic blood pressure was eliminated, whereas those for triglycerides, fasting glucose and insulin, insulin resistance, and systolic blood pressure remained statistically significant. Additional adjustment for BMI further attenuated these associations, and the relation with triglycerides and insulin was no longer statistically significant. Consequently, the associations with metabolic profile may be due in part to an association between yogurt consumption and BMI suggesting that body weight may be an important mediator of these associations. Nonetheless, combined with the null findings for total and HDL cholesterol, our results suggested that yogurt per se may have health benefits partially by affecting the metabolism of glucose but not lipid metabolism. Systolic blood pressure could also be one important target. Future longitudinal studies are warranted to confirm these findings.

Although it has not been clear, the nutrient-dense property of yogurt may shed great light on the potential mechanisms of its health benefits. Especially, vitamins and minerals are essential factors for many metabolic reactions in human body. For example, the shuttle of calcium ion through cell membrane signals numerous cell activities; calcium is also the primary component for bone mineralization. Zinc is a cofactor for many key enzymes. Potassium is the most abundant cation in cells, which participates actively in energy metabolism, membrane transport, and fluid balance. Magnesium serves as an essential cofactor for more than 300 catalytic reactions. B vitamins have a variety of functions in cell growth, division, and metabolism. Therefore, the inadequacy of these micronutrients can be significantly deleterious for a variety of metabolic functions. Many epidemiologic studies also support the importance of these micronutrients. An average 4.7 g/d of potassium intake has been related to 8.0/4.1 mm Hg lower systolic/diastolic blood pressure, 8% to 15% lower risk of cerebrovascular accident, and 6% to 11% lower risk of myocardial infarction [ 38 ]. Higher intake of magnesium has been associated with decreased risk of type II diabetes and metabolic syndrome [ 39 , 40 ]. In this regard, yogurt, as an excellent source of various vitamins and minerals, may be of particular benefit to American diets. On the other hand, the probiotic bacteria in yogurt, although beyond the scope of the current study, may favorably modify the gut micro florae, which play essential roles in energy metabolism, immune function, and metabolic disease [ 32 , 41 ]. In addition, yogurt is a fermented dairy product rich in peptides with in vitro angiotensin-converting enzyme inhibitor effects [ 42 ], which may be one explanation for the association between yogurt consumption and lower systolic blood pressure.

Strengths of the present study included its relatively large study size and consideration of the potential influence of diet quality on the associations between yogurt and nutrient adequacy and metabolic profile. However, some limitations should be also noted. The cross-sectional study design does not indicate any causal inference of yogurt consumption on nutrient adequacy and metabolic profile. The generalizability of our results to other populations of different races or young age groups was also limited because participants were mostly adult white Americans. Although our analyses carefully controlled for the yogurt consumption associated diet quality, latent residual confounding could not be ruled out. In addition, the FFQ did not assess the types of yogurt (eg, low fat or fat free, with or without fruits, supplemented with micronutrients or not, etc), whereas yogurt was generalized in the database as being low fat and with fruit [ 13 ]. Finally, the participants who were excluded were older and less healthy than those who remained in the analyses. To account for the potential confounding effect of age, we adjusted for age in our analyses. However, it is also possible that the differences in age and health status between those who were included and excluded from these analyses may have biased our findings, although the direction of bias is unknown because we do not know the yogurt consumption of those who were excluded.

Overall, as we had hypothesized, yogurt intake was associated with better diet quality with greater intakes of several shortfall nutrients and healthier metabolic profiles in this FHS adult population. Given the low yogurt consumption among general American adults as compared with the European population, increasing yogurt intake among Americans may be promising in helping to achieve greater adequacy for some of the shortfall nutrients and maintain metabolic well-being as part of a healthy, energy-balanced dietary pattern. Future longitudinal studies are warranted to confirm our findings.

Supplementary Material

Acknowledgments.

The authors thank Gail T. Rogers, Jean Mayer USDA Human Nutrition Research Center on Aging at Tufts University, for the help with data set management and Patrice Sutherland, Boston University, for providing the laboratory quality control data.

This work was supported by National Heart, Lung and Blood Institute of the National Institute of Health (contract number: NO1-HC-25195), US Department of Agriculture Agreement 58–1950–7-707, and a research grant from The Dannon Company, Inc.

P. Jacques and H. Wang received support from a grant from The Dannon Company, Inc. K. A. Livingston, C. S. Fox and J. Meigs have no conflict of interest to declare.

Abbreviations

Adequate intake

Body mass index

High-density lipoprotein

Dietary Guidelines for Americans

Dietary guidelines adherence index

Estimated average requirements

Food frequency questionnaire

Framingham Heart Study

Generalized estimating equations

Homeostasis model assessment of insulin resistance

Physical activity index

Appendix A. Supplementary data : Supplementary data to this article can be found online at http://dx.doi.org/10.1016/j.nutres.2012.11.009 .

• 1. The Dietary Guidelines Advisory Committee on the Dietary Guidelines for Americans, 2010. Part D. Section 2: Nutrient Adequacy. [Accessed Mar 2012];Report of the Dietary Guidelines Advisory Committee on the Dietary Guidelines for Americans. 2010 [ Google Scholar ]
• 2. Nicklas TA, O'Neil CE, Fulgoni VL., III The role of dairy in meeting the recommendations for shortfall nutrients in the American diet. J Am Coll Nutr. 2009;28(suppl 1):73S–81S. doi: 10.1080/07315724.2009.10719807. [ DOI ] [ PubMed ] [ Google Scholar ]
• 3. Ranganathan R, Nicklas TA, Yang SJ, Berenson GS. The nutritional impact of dairy product consumption on dietary intakes of adults (1995–1996): the Bogalusa Heart Study. J Am Diet Assoc. 2005;105:1391–400. doi: 10.1016/j.jada.2005.06.024. [ DOI ] [ PubMed ] [ Google Scholar ]
• 4. Fulgoni V, III, Nicholls J, Reed A, Buckley R, Kafer K, Huth P, et al. Dairy consumption and related nutrient intake in African-American adults and children in the United States: continuing survey of food intakes by individuals 1994–1996, 1998, and the National Health And Nutrition Examination Survey 1999–2000. J Am Diet Assoc. 2007;107:256–64. doi: 10.1016/j.jada.2006.11.007. [ DOI ] [ PubMed ] [ Google Scholar ]
• 5. Weinberg LG, Berner LA, Groves JE. Nutrient contributions of dairy foods in the United States, Continuing Survey of Food Intakes by Individuals, 1994–1996, 1998. J Am Diet Assoc. 2004;104:895–902. doi: 10.1016/j.jada.2004.03.017. [ DOI ] [ PubMed ] [ Google Scholar ]
• 6. Foote JA, Murphy SP, Wilkens LR, Basiotis PP, Carlson A. Dietary variety increases the probability of nutrient adequacy among adults. J Nutr. 2004;134:1779–85. doi: 10.1093/jn/134.7.1779. [ DOI ] [ PubMed ] [ Google Scholar ]
• 7. Soedamah-Muthu SS, Ding EL, Al-Delaimy WK, Hu FB, Engberink MF, Willett WC, et al. Milk and dairy consumption and incidence of cardiovascular diseases and all-cause mortality: dose-response meta-analysis of prospective cohort studies. Am J Clin Nutr. 2011;93:158–71. doi: 10.3945/ajcn.2010.29866. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ]
• 8. Tong X, Dong JY, Wu ZW, Li W, Qin LQ. Dairy consumption and risk of type 2 diabetes mellitus: a meta-analysis of cohort studies. Eur J Clin Nutr. 2011;65(9):1027–31. doi: 10.1038/ejcn.2011.62. [ DOI ] [ PubMed ] [ Google Scholar ]
• 9. Ralston RA, Lee JH, Truby H, Palermo CE, Walker KZ. A systematic review and meta-analysis of elevated blood pressure and consumption of dairy foods. J Hum Hypertens. 2012;26(1):3–13. doi: 10.1038/jhh.2011.3. [ DOI ] [ PubMed ] [ Google Scholar ]
• 10. Crichton GE, Bryan J, Buckley J, Murphy KJ. Dairy consumption and metabolic syndrome: a systematic review of findings and methodological issues. Obes Rev. 2011;12:e190–201. doi: 10.1111/j.1467-789X.2010.00837.x. [ DOI ] [ PubMed ] [ Google Scholar ]
• 11. United States Department of Agriculture. Dietary Guidelines for Americans. 2010:78–79. (Policy Document). Released 1/31/11. [ Google Scholar ]
• 12. Buttriss J. Nutritional properties of fermented milk products. Int J Dairy Tech. 1997;50:21–7. [ Google Scholar ]
• 13. [Accessed Mar 2012];National Nutrient Database for Standard Reference, Release 24. 2012 [ Google Scholar ]
• 14. Ivey KL, Lewis JR, Hodgson JM, Zhu K, Dhaliwal SS, Thompson PL, et al. Association between yogurt, milk, and cheese consumption and common carotid artery intima-media thickness and cardiovascular disease risk factors in elderly women. Am J Clin Nutr. 2011;94:234–9. doi: 10.3945/ajcn.111.014159. [ DOI ] [ PubMed ] [ Google Scholar ]
• 15. Mozaffarian D, Hao T, Rimm EB, Willett WC, Hu FB. Changes in diet and lifestyle and long-term weight gain in women and men. N Engl J Med. 2011;364:2392–404. doi: 10.1056/NEJMoa1014296. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ]
• 16. Beydoun MA, Gary TL, Caballero BH, Lawrence RS, Cheskin LJ, Wang Y. Ethnic differences in dairy and related nutrient consumption among US adults and their association with obesity, central obesity, and the metabolic syndrome. Am J Clin Nutr. 2008;87:1914–25. doi: 10.1093/ajcn/87.6.1914. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ]
• 17. Preis SR, Massaro JM, Robins SJ, Hoffmann U, Vasan RS, Irlbeck T, et al. Abdominal subcutaneous and visceral adipose tissue and insulin resistance in the Framingham heart study. Obesity (Silver Spring) 2010;18:2191–8. doi: 10.1038/oby.2010.59. [ DOI ] [ PMC free article ] [ PubMed ] [ Google Scholar ]
• 18. Rimm EB, Giovannucci EL, Stampfer MJ, Colditz GA, Litin LB, Willett WC. Reproducibility and validity of an expanded self-administered semiquantitative food frequency questionnaire among male health professionals. Am J Epidemiol. 1992;135:1114–26. doi: 10.1093/oxfordjournals.aje.a116211. discussion 1127-36. [ DOI ] [ PubMed ] [ Google Scholar ]
• 19. Willett WC, Reynolds RD, Cottrell-Hoehner S, Sampson L, Browne ML. Validation of a semi-quantitative food frequency questionnaire: comparison with a 1-year diet record. J Am Diet Assoc. 1987;87:43–7. [ PubMed ] [ Google Scholar ]
• 20. Salvini S, Hunter DJ, Sampson L, Stampfer MJ, Colditz GA, Rosner B, et al. Food-based validation of a dietary questionnaire: the effects of week-to-week variation in food consumption. Int J Epidemiol. 1989;18:858–67. doi: 10.1093/ije/18.4.858. [ DOI ] [ PubMed ] [ Google Scholar ]
• 21. Fogli-Cawley JJ, Dwyer JT, Saltzman E, McCullough ML, Troy LM, Jacques PF. The 2005 Dietary Guidelines for Americans Adherence Index: development and application. J Nutr. 2006;136:2908–15. doi: 10.1093/jn/136.11.2908. [ DOI ] [ PubMed ] [ Google Scholar ]
• 22. Kannel WB, Sorlie P. Some health benefits of physical activity. The Framingham Study Arch Intern Med. 1979;139:857–61. [ PubMed ] [ Google Scholar ]
• 23. Vasan RS, Beiser A, Seshadri S, Larson MG, Kannel WB, D'Agostino RB, et al. Residual lifetime risk for developing hypertension in middle-aged women and men: The Framingham Heart Study. JAMA. 2002;287:1003–10. doi: 10.1001/jama.287.8.1003. [ DOI ] [ PubMed ] [ Google Scholar ]
• 24. World Health Organization. [Accessed Mar 2012];WHO Expert Committee on Diabetes Mellitus: Second Report. 1980 [ PubMed ] [ Google Scholar ]
• 25. McNamara JR, Schaefer EJ. Automated enzymatic standardized lipid analyses for plasma and lipoprotein fractions. Clin Chim Acta. 1987;166:1–8. doi: 10.1016/0009-8981(87)90188-4. [ DOI ] [ PubMed ] [ Google Scholar ]
• 26. Warnick GR, Benderson J, Albers JJ. Dextran sulfate-Mg2+ precipitation procedure for quantitation of high-density-lipoprotein cholesterol. Clin Chem. 1982;28:1379–88. [ PubMed ] [ Google Scholar ]
• 27. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28:412–9. doi: 10.1007/BF00280883. [ DOI ] [ PubMed ] [ Google Scholar ]
• 28. Food and Nutrition Board. [Accessed Mar 2012];Dietary reference intakes applications in dietary assessment. 2000 [ Google Scholar ]
• 29. Food and Nutrition Board. Dietary reference intakes for vitamin A, vitamin K, arsenic, boron, chromium, copper, iodine, iron, molybdenum, nickel, silicon, vanadium and zinc. Washington DC: National Academy Press; 2001. [ PubMed ] [ Google Scholar ]
• 30. Hjartaker A, Lagiou A, Slimani N, Lund E, Chirlaque MD, Vasilopoulou E, et al. Consumption of dairy products in the European Prospective Investigation into Cancer and Nutrition (EPIC) cohort: data from 35 955 24-hour dietary recalls in 10 European countries. Public Health Nutr. 2002;5:1259–71. doi: 10.1079/PHN2002403. [ DOI ] [ PubMed ] [ Google Scholar ]
• 31. Bourlioux PPP. Nutritional and health properties of yogurt. World Rev Nutr Diet. 1988;56:217–58. doi: 10.1159/000416229. [ DOI ] [ PubMed ] [ Google Scholar ]
• 32. Meydani SN, Ha WK. Immunologic effects of yogurt. Am J Clin Nutr. 2000;71:861–72. doi: 10.1093/ajcn/71.4.861. [ DOI ] [ PubMed ] [ Google Scholar ]
• 33. Food and Nutrition Board Institute of Medicine, National Academies. Dietary Reference Intakes (DRIs): Estimated Average Requirements. 2010 [ Google Scholar ]
• 34. Food and Nutrition Board Institute of Medicine, National Academies. Dietary Reference Intakes (DRIs): Recommended Dietary Allowances and Adequate Intakes, Vitamins. 2010 [ Google Scholar ]
• 35. Smith TM, Kolars JC, Savaiano DA, Levitt MD. Absorption of calcium from milk and yogurt. Am J Clin Nutr. 1985;42:1197–200. doi: 10.1093/ajcn/42.6.1197. [ DOI ] [ PubMed ] [ Google Scholar ]
• 36. Recker RR, Bammi A, Barger-Lux MJ, Heaney RP. Calcium absorbability from milk products, an imitation milk, and calcium carbonate. Am J Clin Nutr. 1988;47:93–5. doi: 10.1093/ajcn/47.1.93. [ DOI ] [ PubMed ] [ Google Scholar ]
• 37. Kolars JC, Levitt MD, Aouji M, Savaiano DA. Yogurt—an autodigesting source of lactose. N Engl J Med. 1984;310:1–3. doi: 10.1056/NEJM198401053100101. [ DOI ] [ PubMed ] [ Google Scholar ]
• 38. Houston MC. The importance of potassium in managing hypertension. Curr Hypertens Rep. 2011;13:309–17. doi: 10.1007/s11906-011-0197-8. [ DOI ] [ PubMed ] [ Google Scholar ]
• 39. Song Y, Manson JE, Buring JE, Liu S. Dietary magnesium intake in relation to plasma insulin levels and risk of type 2 diabetes in women. Diabetes Care. 2004;27:59–65. doi: 10.2337/diacare.27.1.59. [ DOI ] [ PubMed ] [ Google Scholar ]
• 40. McKeown NM, Jacques PF, Zhang XL, Juan W, Sahyoun NR. Dietary magnesium intake is related to metabolic syndrome in older Americans. Eur J Nutr. 2008;47:210–6. doi: 10.1007/s00394-008-0715-x. [ DOI ] [ PubMed ] [ Google Scholar ]
• 41. Cani PD, Delzenne NM. The role of the gut microbiota in energy metabolism and metabolic disease. Curr Pharm Des. 2009;15:1546–58. doi: 10.2174/138161209788168164. [ DOI ] [ PubMed ] [ Google Scholar ]
• 42. Usinger L, Ibsen H, Jensen LT. Does fermented milk possess antihypertensive effect in humans? J Hypertens. 2009;27:1115–20. doi: 10.1097/HJH.0b013e3283292716. [ DOI ] [ PubMed ] [ Google Scholar ]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

• View on publisher site
• PDF (65.1 KB)
• Collections

Similar articles

Cited by other articles, links to ncbi databases.

• Download .nbib .nbib
• Format: AMA APA MLA NLM

Add to Collections

Yogurt and Diabetes: Overview of Recent Observational Studies

Affiliations.

• 1 Human Nutrition Unit, University Hospital of Sant Joan de Reus, Department of Biochemistry and Biotechnology, Faculty of Medicine and Health Sciences, Pere Virgili Health Research Center, Universitat Rovira i Virgili, Reus, Spain; [email protected].
• 2 Biomedical Research Center in Physiopathology of Obesity and Nutrition (CIBERobn), Instituto de Salut Carlos III, Madrid, Spain; and.
• 3 Human Nutrition Unit, University Hospital of Sant Joan de Reus, Department of Biochemistry and Biotechnology, Faculty of Medicine and Health Sciences, Pere Virgili Health Research Center, Universitat Rovira i Virgili, Reus, Spain.
• 4 Department of Nutrition, Harvard T.H. Chan School of Public Health, Boston, MA.
• PMID: 28615384
• DOI: 10.3945/jn.117.248229

The effects of dairy consumption on the prevention of type 2 diabetes remain controversial and depend on the dairy subtype. Yogurt intake has received special attention because its association with health benefits is more consistent than that of other types of dairy products. In the present article, we review those observational studies that evaluated the association between yogurt consumption and type 2 diabetes. We also discuss the possible mechanisms involved in these associations. We found that 13 prospective studies evaluated the association between yogurt intake and type 2 diabetes, most of which showed an inverse association between the frequency of yogurt consumption and the risk of diabetes. In addition to the scientific evidence accumulated from individual prospective studies, several meta-analyses have shown that yogurt consumption has a potential role in diabetes prevention. The most recent analysis shows a 14% lower risk of type 2 diabetes when yogurt consumption was 80-125 g/d compared with no yogurt consumption. The intake of fermented dairy products, especially yogurt, has been inversely associated with variables of glucose metabolism. Yogurt may have probiotic effects that could modulate glucose metabolism. We conclude that yogurt consumption, in the context of a healthy dietary pattern, may reduce the risk of type 2 diabetes in healthy and older adults at high cardiovascular risk. Large-scale intervention studies and randomized clinical trials are warranted to determine if yogurt consumption has beneficial effects on insulin sensitivity and reduces the risk of type 2 diabetes.

Keywords: dairy; fermented dairy products; insulin sensitivity; type 2 diabetes; yogurt.

© 2017 American Society for Nutrition.

Publication types

• Diabetes Mellitus, Type 2 / prevention & control*
• Risk Factors

• Search Menu
• Sign in through your institution
• Advance articles
• Editor's Choice
• Supplement Archive
• Article Collection Archive
• Author Guidelines
• Submission Site
• Open Access
• Call for Papers
• Why Publish?
• About Nutrition Reviews
• About International Life Sciences Institute
• Editorial Board
• Early Career Editorial Board
• Advertising and Corporate Services
• Journals Career Network
• Self-Archiving Policy
• Journals on Oxford Academic
• Books on Oxford Academic

Article Contents

Introduction, fermentation-associated microbes and their journey to the gut, food microbes and colonization resistance, epidemiological evidence of the health benefits of yogurt and other fermented foods, clinical evidence of the health benefits of yogurt and other fermented foods, the special case of yogurt and lactose malabsorption, acknowledgments.

• < Previous

Yogurt and other fermented foods as sources of health-promoting bacteria

• Article contents
• Figures & tables
• Supplementary Data

Car Reen Kok, Robert Hutkins, Yogurt and other fermented foods as sources of health-promoting bacteria, Nutrition Reviews , Volume 76, Issue Supplement_1, 1 December 2018, Pages 4–15, https://doi.org/10.1093/nutrit/nuy056

• Permissions Icon Permissions

Increased consumption of yogurt, kefir, and other fermented foods has been driven, in part, by the health benefits these products may confer. Epidemiological studies have shown that the consumption of fermented foods is associated with reduced risks of type 2 diabetes, metabolic syndrome, and heart disease, along with improved weight management. The microorganisms present in these foods are suggested to contribute to these health benefits. Among these are the yogurt starter culture organisms Streptococcus thermophilus and Lactobacillus delbrueckii subsp bulgaricus as well as Bifidobacterium and Lactobacillus strains that are added for their probiotic properties. In contrast, for other fermented foods, such as sauerkraut, kimchi, and miso, fermentation is initiated by autochthonous microbes present in the raw material. In both cases, for these fermentation-associated microbes to influence the gut microbiome and contribute to host health, they must overcome, at least transiently, colonization resistance and other host defense factors. Culture and culture-independent methods have now clearly established that many of these microbes present in fermented dairy and nondairy foods do reach the gastrointestinal tract. Several studies have shown that consumption of yogurt and other fermented foods may improve intestinal and extraintestinal health and might be useful in improving lactose malabsorption, treating infectious diarrhea, reducing the duration and incidence of respiratory infections, and enhancing immune and anti-inflammatory responses.

For thousands of years, fermented foods have been a major part of the human diet, 1 largely because fermented milk, meat, and plant foods could be better preserved than the fresh raw materials from which they were made. 2 In the absence of drying, salting, or other forms of traditional preservation, perishable foods would spoil or become unsafe to consume. Most fermented foods, in contrast, naturally contain organic acids, ethanol, or other antimicrobial compounds that inhibit the growth of spoilage organisms and foodborne pathogens.

In addition to their enhanced preservation qualities, fermented foods have other attributes that account for their popularity, including unique flavors, textures, and appearances as well as added functionality and economic value. In many parts of the world, fermented foods are among the most important sources of nutrients. 3–5 Cultured dairy products, bread, and fermented sausage, for example, are rich sources of protein, minerals, and vitamins. Fermentation may also reduce the concentration of lactose and other fermentable sugars and increase phenolic compounds that provide antioxidant activity. 6 , 7 Importantly, there is emerging epidemiological and clinical evidence to suggest that the microorganisms responsible for fermentation, along with those added to fermented foods in the form of probiotics, may contribute directly to gastrointestinal and systemic health. 8

The microorganisms that are predominantly involved in the manufacture of fermented dairy, meat, and vegetable products are lactic acid bacteria from the genera Lactobacillus , Streptococcus , Pediococcus , and Leuconostoc . Other bacteria, including acetic acid bacteria, are also important in the fermentation of cocoa beans, vinegar, and kombucha. 9 , 10 , Saccharomyces cerevisiae and other yeasts are widely used in beer, wine, and bread manufacture, and Penicillium spp, Aspergillus spp, and other fungi are used in cheese, fermented meats, and soy-fermented foods. For many foods, bacteria and yeast are combined to produce the desired product. 11 , 12

Although microorganisms are required for the production of the foods mentioned above, not all fermented foods contain live microbes at the time of consumption. For example, lactic acid bacteria and yeast are used in sourdough bread fermentation, but after baking, none of these organisms are present in the finished bread. Similarly, the organisms responsible for wine and beer fermentation are inactivated or physically removed and are absent from the finished product. Nonetheless, vitamins and bioactive molecules produced by the microbes may still be present. In addition, microbes also consume or transform food constituents during fermentation, resulting in compositional changes in the food. However, even in the absence of a heat or separation step, the number of microbes present at the time of consumption depends on the composition, the storage conditions, and the age of the food. 13 , 14

Understanding the molecular basis for the manner in which fermented foods and fermentation-associated microorganisms affect human health has been challenging. However, next-generation sequencing and other molecular methods are now routinely used to identify and assess abundances of microbes present in fermented foods as well as within gastrointestinal microbiomes. 15 , 16 Thus, it is now possible to track specific strains present in fermented foods from consumption to the gastrointestinal tract. 17–19 Transcriptomics, metabolomics, and whole-metagenome sequencing are also being used to identify or predict functional traits of fermentation-associated microorganisms. 20–22

The goal of this review was to assess the nutritional role of live microbes present in fermented foods, with an emphasis on yogurt and other cultured dairy products. The physiological and ecological challenges faced by fermentation-associated and food-related microbes during digestion and transit through the gastrointestinal tract will be described first. Evidence showing that many of these organisms do indeed survive transit will follow. The ability of food-associated microbes to influence the composition of the intestinal microbiota and ameliorate gut imbalances or dysbiosis will be described next. Finally, the health benefits of fermented foods, as reported in epidemiological and clinical studies, will be reviewed. In particular, improved lactose digestion by yogurt bacteria—currently the only approved health claim for a fermented food—will be described.

For food-associated microorganisms to directly influence the intestinal microbiota and improve the nutritional status of the host, they must first traverse several early hurdles 23 ( Figure 1 ). In the mouth, saliva contains enzymes and other antimicrobial constituents, and the oral microbiota itself provides colonization resistance. 24 , 25 In the stomach, gastric pH is usually less than 3.0 (depending on the fasting state), and pepsin, trypsin, and other digestive enzymes effectively degrade cell proteins. 23 Bile salts secreted into the small intestine disrupt cell membranes and contribute to cell permeabilization and death. 26

Challenges faced by food-associated microbes during their transit through the alimentary canal . The presence of proteases, lipases, and other digestive enzymes are initially responsible for the degradation of cell proteins and lipids. The change in pH along the digestive tract also acts as an additional barrier for these microbes. The pH is lowest in the stomach, owing partly to the secretion of hydrochloric acid by the gastric mucosa, and this can be especially detrimental to non–acid-tolerant microbes. Even if these microbes can successfully survive gastric challenges, bile acids are produced by the host in the small intestine, and the residential microbes present in the gastrointestinal tract release short-chain fatty acids. With all these hurdles in place, it is perhaps surprising that so many of these food-associated microbes are still able to survive transit into the colon . Abbreviation : SCFA, small-chain fatty acids.

Detection and recovery of fermentation-associated microbes after ingestion

Abbreviations : CFU, colony-forming units; ITS, internal transcribed spacer; LBS, Lactobacillus selective; MRS, de Man, Rogosa and Sharpe; PES, phenylethyl alcohol sucrose; RSM, reconstituted skim milk; RT-qPCR, quantitative reverse transcriptase polymerase chain reaction; TPY, trypticase phytone yeast extract.

To estimate the number of bacteria recovered from the ileum, the sum of counts was obtained for samples taken at 1-h periods over a duration of 8 h on respective media. Percentages of survival were calculated by dividing the total number of bacteria throughout the collection period by the number of bacteria ingested.

Detection of Bifidobacterium bifidum 1 h after ingestion in both Helicobacter pylori- positive and -negative individuals.

Viable bacterial count extrapolated at 90 min after ingestion.

Viable bacterial count estimated from a graph corresponding to the intake of standardized kimchi.

Samples obtained by other means, including catheters, probes, or biopsy, have been used to assess microbiota communities in the digestive tract and have demonstrated survival of food-associated microbes during digestion ( Table 1 ; 31 ). 39 Ultimately, however, analyses of intestinal microbiomes are most often based on fecal samples. 27 , 34 , 37 Results from such analyses, therefore, reflect the net outcome of a given microbe’s journey through the entire alimentary canal. Thus, when viable cells from fecal samples are enumerated, that measurement is a sum of both cell death and cell growth in the oral cavity, stomach, small intestine, and colon. 23 Experimentally, therefore, it is difficult to determine the actual number or percentage of consumed microorganisms that survived transit into the colon.

Food-associated microbes that have the physiological ability to reach the colon must then contend with the phenomenon of niche exclusion and colonization resistance. Colonization resistance is defined as “resistance to colonization by ingested bacteria or inhibition of overgrowth of resident bacteria normally present at low levels within the intestinal tract.” 40 Collectively, it refers to those antagonistic, ecological, immunological, and structural factors that restrict access of potential new members to an established community ( Figure 2 ; 41 ). 42

Factors linked to the transient nature of food-associated microbes . Colonization resistance has evolved, in part, to protect the host against invading pathogens. However, this phenomenon does not discriminate between pathogenic and nonpathogenic microbes and subjects food-associated microbes to the same resistance that pathogens (in red) encounter either directly or indirectly from the commensal microbiota. The presence of residential microbes that are strongly associated with the mucosal layer may also prevent attachment of other incoming microbes. The latter, therefore, must compete with commensals for adhesion receptors. The residential microbes may also release bacteriocins and other antimicrobial agents that inhibit newly ingested microbes. Microbes must also compete for nutrients, making it difficult for food-associated microbes to fill niches already occupied by commensal microbes. Collectively, the ability of food-associated microbes to evade competitors, tolerate antimicrobial agents, and compete for food and biogeographical niches determines whether these microbes will be able to cause changes in the microbiota. Adapted from Sassone-Corsi and Raffatellu. 41 Abbreviation : SCFA, small-chain fatty acids.

Colonization resistance against invading pathogens is considered one of the primary protective functions of the gastrointestinal microbiota and is mediated in several different ways. 43 Commensal microbes protect the gut lining by providing a physical barrier, and they produce bacteriocins and other antimicrobial agents that inhibit newly arrived competitors. 44 The production of short-chain fatty acids, in particular, lowers the pH and create an unfavorable environment for foreign microbes that are sensitive to low pH. 40 , 45 In general, commensal microbes outcompete transient or allochthonous organisms for nutrients and access to environmental niches. 41 , 46

Even resident organisms such as Clostridium difficile are kept in check by commensal members of the gut microbiota. 47 However, the mechanisms responsible for colonization resistance do not necessarily discriminate between friend and foe. Other potentially beneficial microorganisms, including fermentation-associated lactobacilli, are subject to the same barriers. Thus, most putative probiotic organisms, especially those allochthonous to the gastrointestinal tract, are unsuccessful colonizers and may even be considered ecological invaders. 48–50 In this context, for live microorganisms to be successful invaders, they would need to be introduced in a viable state in high numbers; overcome digestive hurdles and reach the gastrointestinal tract; compete for nutritional resources, grow, and persist; and interact with the resident microbiota to ultimately effect change in the composition or function of the microbiota. 50 , 51 Such are the ecological challenges for probiotics and other food-associated microbes following ingestion.

Despite these limitations, the presence of fermentation microbes in fecal samples is not unusual. For example, lactobacilli are among the most common microbes in fermented foods, and they are also commonly found in human fecal samples, albeit at relatively low abundances. 52–56 Several reports suggest that microorganisms present in diets containing fermented foods may also affect the gut microbiota, at least transiently. 18 , 27 In the study by David et al, 27 participants consumed either plant- or animal-based diets for 5 days, and fecal microbiomes were analyzed before and after treatment by sequencing the 16S rRNA and internal transcribed spacer regions. 27 Cheeses and cured meats were included among the animal-based products that were consumed. Results revealed that diet affected the microbiota, with changes in various taxa and functional traits corresponding to animal- or plant-based diets. Moreover, the researchers detected the presence of microbes (both bacterial and fungal) in the fecal microbiota that were associated with specific fermented foods and their respective starter cultures. The investigators confirmed, on the basis of recovery of either live cells or RNA transcripts, that the fermentation-derived organisms had survived digestion and had reached the colon. Specifically, transcriptomic analysis revealed an increased abundance of Lactococcus lactis , Staphylococcus carnosus , Pediococcus acidilactici , and a Penicillium species in the fecal microbiota derived from an animal-based diet.

In the study by Veiga et al, 18 individuals with irritable bowel syndrome consumed a yogurt-like fermented milk product containing Bifidobacterium animalis twice daily for 4 weeks, and DNA from all of the included strains was detected in fecal samples. Importantly, not only were the abundances of those strains significantly higher than those detected in baseline samples, but the results of metagenomics sequencing also revealed other changes in the microbiota. In particular, Bifidobacterium dentium was increased, whereas 2 pathobionts, Bilophila wadsworthia and Parabacteroides distasonis , were decreased following the dietary treatment. Other unidentified species were also increased, including those capable of producing butyrate and other short-chain fatty acids. The study participants also reported improvement in their irritable bowel syndrome symptoms, suggesting the possibility that the changes in the microbiota might be responsible.

In other studies, the ability of fermentation-associated organisms to survive digestion is more variable, depending on the food consumed and the methods of analysis. In particular, the organisms in yogurt are only occasionally isolated in fecal samples. 57 Thus, while Mater et al 34 and Elli et al 35 reported that S thermophilus or L delbrueckii subsp bulgaricus could be detected by culture-based methods in fecal samples following yogurt consumption, del Campo et al 33 could not recover the yogurt-containing isolates on nutrient agar. However, using a DNA hybridization method, they could detect these organisms in samples from 10 of 96 participants who consumed fresh yogurt. This suggested that the targeted organisms were detectable but not viable in the stool samples. However, it is important to note that the studies from Mater et al 34 and Eli et al 35 used a more selective media to obtain isolates ( Table 1 ). Ideally, isolation followed by the use of molecular methods, whether based on polymerase chain reaction or sequencing, should be employed to identify these isolates at a higher resolution. The presence of fermentation-associated microbes in fecal samples (detected by molecular methods) from individuals who normally consume kimchi, sausage, sauerkraut, and other fermented foods has also been reported. 38 , 52

Shifts in the gut microbiota following antibiotic treatment or other disturbing events may lead to dysbiosis, providing opportunities for growth of pathogenic microbes and onset of disease and inflammation. 58 One way to redress or correct dysbiosis is via ingestion of probiotics, fermented foods, and other dietary sources of beneficial microbes. 59 As noted above, however, ingested microbes encounter considerable environmental challenges on their way to the gut. On the basis of a systematic review of 63 clinical trials, Mcfarland 60 concluded that the ability of probiotic and other food-associated microbes to influence the microbiota and correct dysbiosis was dependent on the individual. Thus, for many people, changes in the gut microbiota were not observed. Nonetheless, probiotic strains that restored a disturbed gut microbiota were more often associated with improved clinical outcomes compared with those strains that had no effect on the microbiota.

Several large epidemiological studies have assessed the effect of consumption of yogurt and other fermented foods on the incidence of various diseases or health outcomes, and many have shown a reduced risk of disease or improvements in health. In one large cohort study of older Mediterranean adults, yogurt-rich diets were associated with a reduced risk of metabolic syndrome. 61 Results from another large prospective study of more than 80 000 Swedish adults suggested that high consumption of cultured milk lowered the risk of developing bladder cancer. 62 The Swedish Malmo Diet and Cancer cohort study also reported reduced risks of cardiovascular disease among individuals who consumed high amounts of fermented milk and among women who consumed cheese. 63 In another large cohort study, less long-term weight gain was associated with yogurt consumption. 64 Similarly, the prospective European Prospective Investigation into Cancer and Nutrition (EPIC) cohort study of European adults revealed that cheese consumption, as well as combined consumption of cheese, yogurt, and fermented milk, was inversely associated with diabetes. 65 Additionally, in the EPIC-Italy cohort of over 45 000 adults, yogurt consumption was associated with a reduced risk of colorectal cancer. 66 However, among the same cohort, consumption of fermented dairy and other foods was not associated with reduced mortality from all causes, cancer, or cardiovascular disease. 67 The possibility exists that yogurt consumers, in general, have a higher overall diet quality than nonconsumers, and this would account for observed differences in metabolic health. However, results from the Quebec Family Study suggested that yogurt consumption was associated with improved health benefits and body composition, independent of diet quality. 68 Finally, it is important to note that, because these studies are based on dietary histories or consumption patterns, it is not possible to determine the type of yogurt consumed. As noted in the next section, many of the commercially marketed yogurts contain strains of probiotic bacteria in addition to the cultures used in yogurt manufacture.

The beneficial effects of fermented foods other than dairy products have also been assessed by epidemiological studies. In Korea, kimchi and other fermented vegetables are among the most widely consumed foods. Results from cross-sectional analyses of adults showed that high consumption (about three 40-g servings per day) of fermented vegetables and other Korean fermented foods was associated with reduced prevalence of asthma and atopic dermatitis. 69 , 70 The reduced rate of type 2 diabetes among Asian populations compared with Western populations was suggested to be due, in part, to the consumption of fermented soybean foods, which are rich in phytoestrogens and bioactive peptides. 71 Likewise, consumption of the fermented soy products miso and natto was also inversely associated with reduced risk of high blood pressure. 72 Interestingly, consumption of tofu, a nonfermented soy product, was not associated with this effect.

According to both tradition and various national and international standards of identity, yogurt is made with a culture containing strains of S thermophilus and L delbrueckii subsp bulgaricus . However, many commercial products are supplemented with probiotic bacteria, particularly strains of Bifidobacterium and Lactobacillus for added benefits . There are a large number of recent human clinical studies in which these so-called probiotic yogurts and other probiotic-containing cultured milk products have been examined, with specific clinical end points measured. 73–79 The effects of yogurt consumption on risk markers of chronic diseases have been recently reviewed. 80 Fewer studies, however, have considered yogurt and other cultured dairy foods that contain only the fermentation-associated microbes as controls. Several of these studies, which assessed the effect of yogurt consumption on glucose tolerance, are described below.

Results from several randomized, controlled trials have shown that probiotic yogurts are generally more effective than conventional yogurts for improving various health outcomes. In one study of 64 type 2 diabetic patients, the effect of probiotic and conventional yogurt consumption on blood glucose and antioxidant status was determined. 81 Compared with the conventional yogurt, the probiotic yogurt decreased fasting blood glucose and increased several measures of antioxidant status. Similar study designs were used to assess insulin resistance in pregnant women, 82 healthy obese women, 83 and patients with nonalcoholic fatty liver disease. 84 The results from all of these studies showed greater changes in serum insulin levels from baseline among individuals consuming probiotic yogurt compared with those consuming conventional yogurt. However, no differences in other physical or physiological changes, such as weight loss and blood pressure, were observed.

Relatively few human clinical studies that examined the effect of fermented vegetables or other fermented foods on health outcomes have been described in the literature. 71 , 85 In part, this is because many of these foods (eg, cruciferous vegetables or soybeans) have nutritional properties independent of fermentation and because fermented foods are ordinarily consumed at relatively low levels. 86 As noted above, however, kimchi is widely consumed in Korea. In a randomized, controlled study of 100 healthy Korean young adults, kimchi consumption resulted in improvements in fasting blood glucose and total cholesterol. 87 Another study with 22 overweight and obese adults showed that fermented kimchi consumption improved fasting blood glucose and other health parameters associated with metabolic syndrome. 88 Finally, similar improvements in obesity parameters (eg, decreased plasma triglyceride levels and triglyceride/high-density lipoprotein ratios) in obese adults were observed following daily consumption of a Korean fermented soybean-based red pepper paste called kochujang. 89

Lactose malabsorption is a condition characterized by the inability of certain individuals to digest lactose. 90 The condition is caused by the poor expression of the enzyme β-galactosidase (lactase), which is ordinarily produced and secreted by the enterocytes that line the small intestine. Although β-galactosidase is ordinarily synthesized during infancy in most individuals, expression of the enzyme is reduced after about 2 to 3 years of age, 91 resulting in a lactase-nonpersistence phenotype. 92 When β-galactosidase is not produced in sufficient levels, lactose remains undigested and passes into the large intestine, where it is fermented by colonic organisms, resulting in the formation of gases and acids and an increase in the osmotic load ( Figure 3 93 ). 91 The resulting symptoms can include diarrhea, gas, and bloating, leading many lactose-intolerant individuals to omit milk and dairy products from their diets. 94 Interestingly, some lactose-intolerant individuals can tolerate modest doses of lactose (up to 12 g), leading some researchers to suggest that the lactose intolerance threshold has been overestimated. 91 Nonetheless, perhaps as much as one-third of the US population and two-thirds of the world population suffer from lactose malabsorption. 95 Lactose digesters, in contrast, express β-galactosidase at sufficient levels such that most of the lactose is hydrolyzed within the jejunum. The resulting glucose and galactose are subsequently absorbed across the epithelial cells and eventually transported into the bloodstream.

Lactose digestion in lactose-tolerant individuals and in lactose maldigesters following yogurt consumption. Lactose-tolerant individuals (left panel) hydrolyze lactose via β-galactosidase secreted in the small intestine, and the end products, glucose and galactose, are absorbed. Lactose maldigesters (center panel) do not secrete sufficient levels of β-galactosidase, and lactose reaches the colon intact, where it causes colonic distress (acid and gas). When yogurt is consumed (right panel), Streptococcus thermophilus (St) and Lactobacillus delbrueckii subsp bulgaricus (Lb) produce β-galactosidase in the small intestine, and lactose hydrolysis is restored. Adapted from Hutkins. 93 Abbreviations : E, β-galactosidase; Gal, galactose; Glu, glucose; Lac, lactose; Lb, Lactobacillus delbrueckii subsp bulgaricus ; St, Streptococcus thermophilus .

Most lactose-intolerant individuals are able to eat yogurt without developing symptoms, and yogurt consumption is often recommended as a suitable dietary strategy for these individuals. 96 That yogurt, but not acidified milk or heat-treated yogurt, is tolerated by lactose-intolerant individuals suggests that the microbes in yogurt have a protective effect against lactose. 97–99 Specifically, the yogurt culture organisms S thermophilus and L delbrueckii subsp bulgaricus produce β-galactosidase as part of their lactose utilization pathway and can potentially improve lactose digestion in vivo. 100 Note that the lactose content is only partially reduced by the actual fermentation of yogurt, with most lactose remaining intact in the finished product. When yogurt is consumed, the live organisms, which contain intracellular β-galactosidase, presumably survive the acidic conditions in the stomach and reach the small intestine. There, they are likely permeabilized by bile acids, releasing β-galactosidase into the lumen. 7 , 101 Thus, the lactose is hydrolyzed by bacterial β-galactosidase and the monosaccharides are absorbed across the intestinal epithelium.

Several systematic reviews have reported that probiotic microorganisms, including S thermophilus and L delbrueckii subsp bulgaricus , vary in their ability to improve lactose digestion and reduce symptoms of lactose maldigestion. 102–104 The European Food Safety Authority also reviewed human clinical studies that assessed the effectiveness of yogurt in enhancing lactose digestion and reducing symptoms of lactose intolerance. 105 The expert panel reached the following conclusions: (1) there was “strong evidence for the biological plausibility of the effect”; and (2) a cause-and-effect relationship between yogurt consumption and improved lactose digestion was sufficiently established to warrant a health claim, provided the yogurt contained at least 10 8 colony-forming units (CFU) per gram.

Interestingly, sour cream and cultured buttermilk contain comparable levels of lactose. These, as well as other fermented dairy products, are made using cultures containing mesophilic species of Lactococcus and Leuconostoc , yet neither is well tolerated by lactose-intolerant individuals. 106 , 107 This is evidently because these bacteria do not express β-galactosidase. Instead, lactococci metabolize lactose via a β-galactosidase-independent pathway. 108 Specifically, they express the enzyme phospho-β-galactosidase, whose substrate is lactose phosphate. Lactose phosphate is formed via a phosphotransferase pathway that phosphorylates lactose during its transport across an intact cell membrane. Thus, free lactose is not hydrolyzed by this enzyme.

Hygienic lifestyles and diets low in fermented foods are among the factors that have likely reduced exposure to environment- and food-associated microbes and may contribute, in part, to intestinal dysbiosis. 109 The hypothesis that diets rich in fermented foods containing live organisms could redress a dysbiotic intestinal microbiota is an attractive proposition, but it is not new. More than 100 years ago, the Nobel laureate Ilya Metchnikoff wrote the following prescient passage: “The dependence of the intestinal microbes on the food makes it possible to adopt measures to modify the flora in our bodies and to replace the harmful microbes by useful microbes.”

However, as Metchnikoff also noted, the absence of suitable methods was a major challenge. “Unfortunately, our actual knowledge of the intestinal flora is still very imperfect because of the impossibility of finding artificial media in which it could be grown. Notwithstanding this difficulty, however, a rational solution of the problem must be sought.”

In 2018, these impediments no longer exist, and the microbiomes from gastrointestinal as well as food environments are now routinely surveyed. Indeed, as Veiga et al 18 recently noted, the role of food- or fermentation-derived microbes in promoting gut and systemic health has likely been under-reported because of methodological limitations. Humans have been estimated to ingest as many as 10 9 to 10 12 CFU per day. 23 , 110 Although this amount includes microbes from a range of food sources, diets rich in fermented foods likely contribute a large portion of the total. 59 Evidence is accumulating that the allochthonous bacteria in fermented foods, despite their transient occurrence in the gastrointestinal tract, can nonetheless influence the resident microbiome and exert host-specific health benefits. 19 , 23 , 59

We thank Mary Ellen Sanders and Densie Webb for constructive comments.

Author contributions . Both authors contributed equally to the manuscript.

Funding/support . C.K. was supported by a grant from Mead Johnson Nutrition. R.H. received travel expenses and an honorarium from the Danone Institute for delivering a lecture at the Fifth International Yogurt Summit at the International Congress of Nutrition in October 2017.

Declaration of interest . R.H. has received grants and honoraria from several food and ingredient companies, is a co-owner of Synbiotic Solutions, LLC, and is on the board of directors of the International Scientific Association for Probiotics and Prebiotics.

Chilton SN , Burton JP , Reid G. Inclusion of fermented foods in food guides around the world . Nutrients . 2015 ; 7 : 390 – 404 .

Google Scholar

Ross RP , Morgan S , Hill C. Preservation and fermentation: past, present and future . Int J Food Microbiol . 2002 ; 79 : 3 – 16 .

Marsh AJ , Hill C , Ross RP , et al. . Fermented beverages with health-promoting potential: past and future perspectives . Trends Food Sci Technol . 2014 ; 38 : 113 – 124 .

Marco ML , Golomb BL. Fermented foods, Lactobacillus , and health . Microbe . 2016 ; 11 : 349 – 354 .

Tremblay A , Panahi S. Yogurt consumption as a signature of a healthy diet and lifestyle . J Nutr. 2017 ; 147 : 1476S – 1480S .

Sacchi KL , Bisson LF , Adams DO. A review of the effect of winemaking techniques on phenolic extraction in red wines . Am J Enol Vitic . 2005 ; 56 : 197 – 206 .

Shah NP. Health benefits of yogurt and fermented milk. In: Chandan RC , ed. Manufacturing Yogurt and Fermented Milks . Ames, IA : Blackwell Publishing ; 2006 : 327 – 340 .

Google Preview

Marco ML , Heeney D , Binda S , et al. . Health benefits of fermented foods: microbiota and beyond . Curr Opin Biotechnol. 2017 ; 44 : 94 – 102 .

Meersman E , Steensels J , Mathawan M , et al. . Detailed analysis of the microbial population in Malaysian spontaneous cocoa pulp fermentations reveals a core and variable microbiota . PLoS One . 2013 ; 8 : e81559. doi: 10.1371/journal.pone.0081559

De Roos J , De Vuyst L. Acetic acid bacteria in fermented foods and beverages . Curr Opin Biotechnol. 2018 ; 49 : 115 – 119 .

Sieuwerts S , Bron PA , Smid EJ. Mutually stimulating interactions between lactic acid bacteria and Saccharomyces cerevisiae in sourdough fermentation . LWT Food Sci Technol . 2018 ; 90 : 201 – 206 .

Liu Y , Rousseaux S , Tourdot-Maréchal R , et al. . Wine microbiome: a dynamic world of microbial interactions . Crit Rev Food Sci Nutr. 2015 ; 57 : 856 – 873 .

Chang JY , Chang HC. Improvements in the quality and shelf life of kimchi by fermentation with the induced bacteriocin-producing strain, Leuconostoc citreum GJ7 as a starter . Food Microbiol Saf . 2010 ; 75 : M103 – M110 .

Zhi N-N , Zong K , Thakur K , et al. . Development of a dynamic prediction model for shelf-life evaluation of yogurt by using physicochemical, microbiological and sensory parameters . CYTA J Food . 2017 ; 16 : 42 – 49 .

Ercolini D. Exciting strain-level resolution studies of the food microbiome . Microb Biotechnol. 2017 ; 10 : 54 – 56 .

Macori G , Cotter PD. Novel insights into the microbiology of fermented dairy foods . Curr Opin Biotechnol . 2018 ; 49 : 172 – 178 .

McNulty NP , Yatsunenko T , Hsiao A , et al. . The impact of a consortium of fermented milk strains on the gut microbiome of gnotobiotic mice and monozygotic twins . Sci Transl Med . 2011 ; 3 : 106ra106. doi: 10.1126/scitranslmed.3002701

Veiga P , Pons N , Agrawal A , et al. . Changes of the human gut microbiome induced by a fermented milk product . Sci Rep. 2014 ; 4 : 6328. doi: 10.1038/srep06328

Zhang C , Derrien M , Levenez F , et al. . Ecological robustness of the gut microbiota in response to ingestion of transient food-borne microbes . ISME J. 2016 ; 10 : 2235 – 2245 .

Cao Y , Fanning S , Proos S , et al. . A review on the applications of next generation sequencing technologies as applied to food-related microbiome studies . Front Microbiol. 2017 ; 8 : 1829. doi: 10.3389/fmicb.2017.01829

De Filippis F , Parente E , Ercolini D. Metagenomics insights into food fermentations . Microb Biotechnol. 2017 ; 10 : 91 – 102 .

Pimentel G , Burton KJ , Vergères G , et al. . The role of foodomics to understand the digestion/bioactivity relationship of food . Curr Opin Food Sci . 2018 ; 22 : 67 – 73 .

Derrien M , van Hylckama Vlieg JET. Fate, activity, and impact of ingested bacteria within the human gut microbiota . Trends Microbiol . 2015 ; 23 : 354 – 366 .

Kilian M , Chapple ILC , Hannig M , et al. . The oral microbiome—an update for oral healthcare professionals . Br Dent J. 2016 ; 221 : 657 – 666 .

Marsh PD , Do T , Beighton D , et al. . Influence of saliva on the oral microbiota . Periodontol 2000. 2016 ; 70 : 80 – 92 .

Begley M , Gahan CGM , Hill C. The interaction between bacteria and bile . FEMS Microbiol Rev. 2005 ; 29 : 625 – 651 .

David LA , Maurice CF , Carmody RN , et al. . Diet rapidly and reproducibly alters the human gut microbiome . Nature . 2014 ; 505 : 559 – 563 .

Pochart P , Marteau P , Bouhnik Y , et al. . Survival of bifidobacteria ingested via fermented milk during their passage through the human small intestine: an in vivo study using intestinal perfusion . Am J Clin Nutr . 1992 ; 55 : 78 – 80 .

Oozeer R , Leplingard A , Mater DDGG , et al. . Survival of Lactobacillus casei in the human digestive tract after consumption of fermented milk . Appl Environ Microbiol . 2006 ; 72 : 5615 – 5617 .

Vesa T , Pochart P , Marteau P. Pharmacokinetics of Lactobacillus plantarum NCIMB 8826, Lactobacillus fermentum KLD, and Lactococcus lactis MG 1363 in the human gastrointestinal tract . Aliment Pharmacol Ther . 2000 ; 14 : 823 – 828 .

Shibahara-Sone H , Gomi A , Iino T , et al. . Living cells of probiotic Bifidobacterium bifidum YIT 10347 detected on gastric mucosa in humans . Benef Microbes . 2016 ; 7 : 319 – 326 .

Pochart P , Dewit O , Desjeux JF , et al. . Viable starter culture, β-galactosidase activity, and lactose in duodenum after yogurt ingestion in lactase-deficient humans . Am J Clin Nutr . 1989 ; 49 : 828 – 831 .

del Campo R , Bravo D , Cantón R , et al. . Scarce evidence of yogurt lactic acid bacteria in human feces after daily yogurt consumption by healthy volunteers . Appl Environ Microbiol . 2005 ; 71 : 547 – 549 .

Mater DDG , Bretigny L , Firmesse O , et al. . Streptococcus thermophilus and Lactobacillus delbrueckii subsp. bulgaricus survive gastrointestinal transit of healthy volunteers consuming yogurt . FEMS Microbiol Lett . 2005 ; 250 : 185 – 187 .

Elli M , Callegari ML , Ferrari S , et al. . Survival of yogurt bacteria in the human gut . Appl Environ Microbiol . 2006 ; 72 : 5113 – 5117 .

Kil J-H , Jung K-O , Lee H-S , et al. . Effects of kimchi on stomach and colon health of Helicobacter pylori -infected volunteers . J Food Sci Nutr. 2004 ; 9 : 161 – 166 .

Lee KE , Cho UH , Ji GE. Effect of kimchi intake on the composition of human large intestinal bacteria . Korean J Food Sci Technol . 1996 ; 28 : 981 – 986 .

Han K , Bose S , Wang J , et al. . Contrasting effects of fresh and fermented kimchi consumption on gut microbiota composition and gene expression related to metabolic syndrome in obese Korean women . Mol Nutr Food Res. 2015 ; 59 : 1004 – 1008 .

Zilberstein B , Quintanilha AG , Santos MAA , et al. . Digestive tract microbiota in healthy volunteers . Clinics . 2007 ; 62 : 47 – 54 .

Lawley TD , Walker AW. Intestinal colonization resistance . Immunology . 2012 ; 138 : 1 – 11 .

Sassone-Corsi M , Raffatellu M. No vacancy: how beneficial microbes cooperate with immunity to provide colonization resistance to pathogens . J Immunol. 2015 ; 194 : 4081 – 4087 .

He X , McLean JS , Guo L , et al. . The social structure of microbial community involved in colonization resistance . ISME J. 2014 ; 8 : 564 – 574 .

Mullineaux-Sanders C , Suez J , Elinav E , et al. . Sieving through gut models of colonization resistance . Nat Microbiol. 2018 ; 3 : 132 – 140 .

Dobson A , Cotter PD , Ross RP , et al. . Bacteriocin production as a probiotic trait? Appl Environ Microbiol. 2012 ; 78 : 1 – 6 .

Looijer–Van Langen MAC , Dieleman LA. Prebiotics in chronic intestinal inflammation . Inflamm Bowel Dis. 2009 ; 15 : 454 – 462 .

Buffie CG , Pamer EG. Microbiota-mediated colonization resistance against intestinal pathogens . Nat Rev Immunol. 2013 ; 13 : 790 – 801 .

Schubert AM , Sinani H , Schloss PD. Antibiotic-induced alterations of the murine gut microbiota and subsequent effects on colonization resistance against Clostridium difficile . MBio . 2015 ; 6 : e00974 . doi: 10.1128/mBio.00974-15

Murall CL , Abbate JL , Puelma Touzel M , et al. . Invasions of host-associated microbiome networks . Adv Ecol Res . 2017 ; 57 : 201 – 281 . doi:10.1016/bs.aecr.2016.11.002

Preidis GA , Hill C , Guerrant RL , et al. . Probiotics, enteric and diarrheal diseases, and global health . Gastroenterology . 2011 ; 140 : 8 – 14 .

Walter J , Maldonado-Gómez MX , Martínez I. To engraft or not to engraft: an ecological framework for gut microbiome modulation with live microbes . Curr Opin Biotechnol . 2018 ; 49 : 129 – 139 .

Mallon CA , van Elsas JD , Salles JF. Microbial invasions: the process, patterns, and mechanisms . Trends Microbiol . 2015 ; 23 : 719 – 729 .

Dal Bello F , Walter J , Hammes WP , et al. . Increased complexity of the species composition of lactic acid bacteria in human feces revealed by alternative incubation condition . Microb Ecol . 2003 ; 45 : 455 – 463 .

Walter J , Hertel C , Tannock GW , et al. . Detection of Lactobacillus , Pediococcus , Leuconostoc , and Weissella species in human feces by using group-specific PCR primers and denaturing gradient gel electrophoresis . Appl Environ Microbiol . 2001 ; 67 : 2578 – 2585 .

Park KY , Jeong JK. Health benefits of kimchi (Korean fermented vegetables) as a probiotic food . J Med Food. 2014 ; 17 : 6 – 20 .

Lebeer S , Bron PA , Marco ML , et al. . Identification of probiotic effector molecules: present state and future perspectives . Curr Opin Biotechnol. 2018 ; 49 : 217 – 223 .

Heeney DD , Gareau MG , Marco ML. Intestinal Lactobacillus in health and disease, a driver or just along for the ride? Curr Opin Biotechnol. 2018 ; 49 : 140 – 147 .

Morelli L. Yogurt, living cultures, and gut health . Am J Clin Nutr. 2014 ; 99(5 suppl) : 1248S – 1250S .

Arnold JW , Roach J , Azcarate-Peril MA. Emerging technologies for gut microbiome research . Trends Microbiol. 2016 ; 24 : 887 – 901 .

Plé C , Breton J , Daniel C , et al. . Maintaining gut ecosystems for health: are transitory food bugs stowaways or part of the crew? Int J Food Microbiol. 2015 ; 213 : 139 – 143 .

McFarland LV. Use of probiotics to correct dysbiosis of normal microbiota following disease or disruptive events: a systematic review . BMJ Open . 2014 ; 4 : e005047. doi: 10.1136/bmjopen-2014-005047

Babio N , Becerra-Tomas N , Martinez-Gonzalez MA , et al. . Consumption of yogurt, low-fat milk, and other low-fat dairy products is associated with lower risk of metabolic syndrome incidence in an elderly Mediterranean population . J Nutr . 2015 ; 145 : 2308 – 2316 .

Larsson SC , Andersson S , Johansson JE , et al. . Cultured milk, yogurt, and dairy intake in relation to bladder cancer risk in a prospective study of Swedish women and men . Am J Clin Nutr. 2008 ; 88 : 1083 – 1087 .

Sonestedt E , Wirfält E , Wallström P , et al. . Dairy products and its association with incidence of cardiovascular disease: the Malmö Diet and Cancer Cohort . Eur J Epidemiol. 2011 ; 26 : 609 – 618 .

Mozaffarian D , Hao T , Rimm EB , et al. . Changes in diet and lifestyle and long- term weight gain in women and men . N Engl J Med. 2011 ; 364 : 2392 – 2404 .

Sluijs I , Forouhi NG , Beulens JW , et al. . The amount and type of dairy product intake and incident type 2 diabetes: results from the EPIC-InterAct Study . Am J Clin Nutr . 2012 ; 96 : 382 – 390 .

Pala V , Sieri S , Berrino F , et al. . Yogurt consumption and risk of colorectal cancer in the Italian European Prospective Investigation into Cancer and Nutrition cohort . Int J Cancer. 2011 ; 129 : 2712 – 2719 .

Praagman J , Dalmeijer GW , van der Schouw YT , et al. . The relationship between fermented food intake and mortality risk in the European Prospective Investigation into Cancer and Nutrition-Netherlands cohort . Br J Nutr. 2015 ; 113 : 498 – 506 .

Panahi S , Doyon CY , Després J , et al. . Yogurt consumption, body composition, and metabolic health in the Québec Family Study . Eur J Nutr 2018 ; 57 : 1591 – 1603 . doi:10.1007/s00394-017-1444-9

Kim HJ , Ju S , Park YK. Kimchi intake and atopic dermatitis in Korean aged 19-49 years: the Korea National Health and Nutrition Examination Survey 2010-2012 . Asia Pac J Clin Nutr . 2017 ; 26 : 914 – 922 . doi:10.6133/apjcn.022017.16

Park S , Bae JH. Fermented food intake is associated with a reduced likelihood of atopic dermatitis in an adult population (Korean National Health and Nutrition Examination Survey 2012-2013) . Nutr Res . 2016 ; 36 : 125 – 133 .

Kwon DY , Daily JW III , Kim HJ , et al. . Antidiabetic effects of fermented soybean products on type 2 diabetes . Nutr Res. 2010 ; 30 : 1 – 13 .

Nozue M , Shimazu T , Sasazuki S , et al. . Fermented soy product intake is inversely associated with the development of high blood pressure: the Japan Public Health Center-Based Prospective Study . J Nutr . 2017 ; 147 : 1749 – 1756 .

Burton KJ , Rosikiewicz M , Pimentel G , et al. . Probiotic yogurt and acidified milk similarly reduce postprandial inflammation and both alter the gut microbiota of healthy, young men . Br J Nutr. 2017 ; 117 : 1312 – 1322 .

Pei R , Dimarco DM , Putt KK , et al. . Low-fat yogurt consumption reduces biomarkers of chronic inflammation and inhibits markers of endotoxin exposure in healthy premenopausal women: a randomised controlled trial . Br J Nutr. 2017 ; 118 : 1043 – 1051 .

Burton KJ , Gory Pimentel G , Zangger N , et al. . Modulation of the peripheral blood transcriptome by the ingestion of probiotic yoghurt and acidified milk in healthy, young men . PLoS One. 2018 ; 13 : e0192947 . doi: 10.1371/journal.pone.0192947

Pimentel G , Burton KJ , Rosikiewicz M , et al. . Blood lactose after dairy product intake in healthy men . Br J Nutr. 2017 ; 118 : 1070 – 1077 .

Laue C , Papazova E , Liesegang A , et al. . Effect of a yoghurt drink containing Lactobacillus strains on bacterial vaginosis in women—a double-blind, randomised, controlled clinical pilot trial . Benef Microbes . 2018 ; 9 : 35 – 50 .

Pu F , Guo Y , Li M , et al. . Yogurt supplemented with probiotics can protect the healthy elderly from respiratory infections: a randomized controlled open-label trial . Clin Interv Aging. 2017 ; 12 :1223 – 1231 .

Fox MJ , Ahuja KDK , Robertson IK , et al. . Can probiotic yogurt prevent diarrhoea in children on antibiotics? A double- blind, randomised, placebo-controlled study . Br Med J . 2015 ; 5 : e006474. doi: 10.1136/bmjopen-2014-006474

Dumas A , Lapointe A , Dugrenier M , et al. . A systematic review of the effect of yogurt consumption on chronic diseases risk markers in adults . Eur J Nutr. 2017 ; 56 : 1375 – 1392 .

Ejtahed HS , Mohtadi-Nia J , Homayouni-Rad A , et al. . Probiotic yogurt improves antioxidant status in type 2 diabetic patients . Nutrition . 2012 ; 28 : 539 – 543 .

Asemi Z , Samimi M , Tabassi Z , et al. . Effect of daily consumption of probiotic yoghurt on insulin resistance in pregnant women: a randomized controlled trial . Eur J Clin Nutr. 2013 ; 67 : 71 – 74 .

Madjd A , Taylor MA , Mousavi N , et al. . Comparison of the effect of daily consumption of probiotic compared with low-fat conventional yogurt on weight loss in healthy obese women following an energy-restricted diet: a randomized controlled trial . Am J Clin Nutr . 2016 ; 103 : 323 – 329 .

Nabavi S , Rafraf M , Somi M-H , et al. . Probiotic yogurt improves body mass index and fasting insulin levels without affecting serum leptin and adiponectin levels in non-alcoholic fatty liver disease (NAFLD) . J Funct Foods . 2015 ; 18 : 684 – 691 .

Peñas E , Martinez-Villaluenga C , Frias J. Sauerkraut: production, composition, and health benefits. In: Frias J , Martinez-Villaluenga C , Peñas , eds. Fermented Foods in Health and Disease Prevention . 1st ed. New York, NY : Elsevier ; 2016 : 557 – 576 .

Zieliński H , Surma M , Zielińska D. The naturally fermented sour pickled cucumbers. In: Frias J , Martinez-Villaluenga C , Peñas , eds. Fermented Foods in Health and Disease Prevention . 1st ed. New York, NY : Elsevier ; 2016 : 503 – 516 .

Choi IH , Noh JS , Han J-S , et al. . Kimchi, a fermented vegetable, improves serum lipid profiles in healthy young adults: randomized clinical trial . J Med Food . 2013 ; 16 : 223 – 229 .

Kim EK , An SY , Lee MS , et al. . Fermented kimchi reduces body weight and improves metabolic parameters in overweight and obese patients . Nutr Res. 2011 ; 31 : 436 – 443 .

Lee Y , Cha YS , Park Y , et al. . PPARγ2 C1431T polymorphism interacts with the antiobesogenic effects of Kochujang, a Korean fermented, soybean-based red pepper paste, in overweight/obese subjects: a 12-week, double-blind randomized clinical trial . J Med Food . 2017 ; 20 : 610 – 617 .

Savaiano DA. Lactose digestion from yogurt: mechanism and relevance . Am J Clin Nutr. 2014 ; 99(5 suppl) : 1251S – 1255S .

Corgneau M , Scher J , Ritie-Pertusa L , et al. . Recent advances on lactose intolerance: tolerance thresholds and currently available answers . Crit Rev Food Sci Nutr. 2017 ; 57 : 3344 – 3356 .

Heine RG , Alrefaee F , Bachina P , et al. . Lactose intolerance and gastrointestinal cow’s milk allergy in infants and children—common misconceptions revisited . World Allergy Organ J. 2017 ; 10 : 41. doi: 10.1186/s40413-017-0173-0

Hutkins RW. Microbiology and Technology of Fermented Foods. 2nd edn. Hoboken, NJ : Wiley . In press.

Ingram CJE , Mulcare CA , Itan Y , et al. . Lactose digestion and the evolutionary genetics of lactase persistence . Hum Genet. 2009 ; 124 : 579 – 591 .

Storhaug CL , Fosse SK , Fadnes LT. Country, regional, and global estimates for lactose malabsorption in adults: a systematic review and meta-analysis . Lancet Gastroenterol Hepatol . 2017 ; 2 : 738 – 746 .

Hertzler S , Savaiano DA , Dilk A , et al. . Nutrient considerations in lactose intolerance. In: Coulston A , Boushey C , Ferruzzi M , Delahanty L , eds. 4th ed. Nutrition in the Prevention and Treatment of Disease . New York, NY : Elsevier ; 2017 : 875 – 892 .

Kolars JC , Michael DL , Aouji M , et al. . Yogurt—an autodigesting source of lactose . N Engl J Med. 1984 ; 310 : 1 – 3 .

Martini MC , Bollweg GL , Levitt MD , et al. . Lactose digestion by yogurt beta-galactosidase: influence of pH and microbial cell integrity . Am J Clin Nutr. 1987 ; 45 : 432 – 436 .

Pelletier X , Laure-Boussuge S , Donazzolo Y. Hydrogen excretion upon ingestion of dairy products in lactose- intolerant male subjects: importance of the live flora . Eur J Clin Nutr. 2001 ; 55 : 509 – 512 .

Martini MC , Lerebours EC , Lin W-J , et al. . Strains and species of lactic acid bacteria in fermented milks (yogurts): effect on in vivo lactose digestion . Am J Clin Nutr. 1991 ; 54 : 1041 – 1046 .

de Vrese M , Stegelmann A , Richter B , et al. . Probiotics—compensation for lactase insufficiency . Am J Clin Nutr. 2001 ; 73(2 suppl) : 421S – 429S .

Levri KM , Ketvertis K , Deramo M , et al. . Do probiotics reduce adult lactose intolerance? A systematic review . J Fam Pract. 2005 ; 54 : 613 – 620 .

Oak SJ , Jha R. The effects of probiotics in lactose intolerance: a systematic review . Crit Rev Food Sci Nutr . 2018 ; 1 – 9 .

Shaukat A , Levitt MD , Taylor BC , et al. . Systematic review: effective management strategies for lactose intolerance . Ann Intern Med. 2010 ; 152 : 797 – 803 .

EFSA Panel on Dietetic Products, Nutrition, and Allergies . Scientific Opinion on the substantiation of health claims related to live yoghurt cultures and improved lactose digestion (ID 1143, 2976) pursuant to Article 13(1) of Regulation (EC) No. 1924/2006 . EFSA J. 2010 ; 8 : 1763. doi: 10.2903/j.efsa.2010.1763

Lovelace HY , Barr SI. Diagnosis, symptoms, and calcium intakes of individuals with self-reported lactose intolerance . J Am Coll Nutr. 2005 ; 24 : 51 – 57 .

Savaiano DA , AbouElAnouar A , Smith DE , et al. . Lactose malabsorption from yogurt, pasteurized yogurt, sweet acidophilus milk, and cultured milk in lactase-deficient individuals . Am J Clin Nutr . 1984 ; 40 : 1219 – 1223 .

McAuliffe O. Genetics of Lactic Acid Bacteria . In: McSweeney PLH , Fox PF , Cotter PD , Everett DW , eds. 4th ed. Cheese . New York, NY : Elsevier ; 2017 : 227 – 247 .

Karkman A , Lehtimäki J , Ruokolainen L. The ecology of human microbiota: dynamics and diversity in health and disease . Ann N Y Acad Sci. 2017 ; 1399 : 78 – 92 .

Lang JM , Eisen JA , Zivkovic AM. The microbes we eat: abundance and taxonomy of microbes consumed in a day’s worth of meals for three diet types . PeerJ . 2014 ; 2 : e659. doi:10.7717/peerj.659

• fermentation
• microorganisms
• microbial colonization
• fermented foods

Email alerts

Citing articles via.

• X (formerly Twitter)
• Recommend to your Library

Affiliations

• Online ISSN 1753-4887
• Print ISSN 0029-6643
• Copyright © 2024 International Life Sciences Institute
• About Oxford Academic
• Publish journals with us
• University press partners
• What we publish
• New features  
• Open access
• Institutional account management
• Rights and permissions
• Get help with access
• Accessibility
• Advertising
• Media enquiries
• Oxford University Press
• Oxford Languages
• University of Oxford

Oxford University Press is a department of the University of Oxford. It furthers the University's objective of excellence in research, scholarship, and education by publishing worldwide

• Copyright © 2024 Oxford University Press
• Cookie settings
• Cookie policy
• Privacy policy
• Legal notice

This Feature Is Available To Subscribers Only

Sign In or Create an Account

This PDF is available to Subscribers Only

For full access to this pdf, sign in to an existing account, or purchase an annual subscription.