Potential benefits of fruit and yogurt thanks to their probiotic and prebiotic properties

Dec 13, 2022Derry Procaccini
Potenziali benefici di frutta e yogurt grazie alle loro proprietà probiotiche e prebiotiche

Fruit and yogurt have been individually identified as indicators of healthy eating patterns.

Fruits have a relatively low energy density and are an excellent source of antioxidants, prebiotic fiber, and polyphenols, which can support digestive health. Yogurt, on the other hand, is a nutrient-dense food that is a good source of milk protein, calcium, magnesium, vitamin B-12, conjugated linoleic acid, and other key fatty acids. Additionally, it contains beneficial bacterial cultures, making it a potential source of probiotics. The unique fermented food matrix of yogurt provides additional health benefits by improving nutrient absorption and digestion. The combination of yogurt and fruit intake may provide probiotics, prebiotics, high-quality protein, important fatty acids, and a blend of vitamins and minerals that have the potential to exert synergistic effects on health. Yogurt consumption has been associated with reduced weight gain and a lower incidence of type 2 diabetes, while fruit has established effects on reducing the risk of cardiovascular disease. Yogurt and fruit can be consumed together and may exert combined health benefits through potential prebiotic and probiotic effects. Furthermore, replacing high-energy, nutrient-poor snacks with fruit and yogurt may reduce the intake of high-calorie obesogenic foods. Given the positive cardiometabolic impacts of fruit and yogurt and their association with healthy dietary patterns, there is sufficient evidence to warrant further exploration of the potential synergistic health benefits of combined fruit and yogurt intake.

Introduction

It has long been known that fruits, vegetables, and dairy products are healthful components of the diet, as demonstrated by their inclusion in national food guides and nutritional guidelines worldwide ( 1 , 2 ). More recently, it has been suggested that whole plant foods, probiotics, and prebiotics may modulate the microbiota, leading to cardiac health ( 3 ). From publications studying the effects of diet on health, consistent healthy dietary patterns have been elucidated across diverse populations. For example, A fruit and dairy pattern has been linked to a lower risk of metabolic syndrome in Korean adults ( 4 ), and A diet rich in fruits, vegetables, and low-fat dairy products was effective in reducing blood pressure in American adults ( 5 , 6 ). Studying food consumption patterns is likely to better reflect the complex synergistic benefits of consuming different foods together, rather than studying the health outcomes of individual foods and nutrients ( 7 ). Diet quality indices and healthy dietary pattern analyses are important methods used to decode the complexity of the diet and its association with health outcomes that go beyond individual nutrients. Given the complex nature of dietary variables, multiple analytical approaches are called upon to investigate the relationship between dietary risk and disease ( 8 ). Aside from dietary patterns and individual food and nutrient analyses, food combination synergies are an approach to diet analysis that takes the food matrix into account, thus warranting investigation.

Food matrix creates nutritional synergy

It has been suggested that the food matrix, which combines nutrients in a specific structural arrangement, may endow a food with a synergy of properties that would not be available if the individual nutrients were consumed separately ( 9 ).

Yogurt and fruit have been identified in isolation to exert protective effects against specific diet-related diseases (DRDs) 8 , such as type 2 diabetes (T2D) ( 10 , 11 ). These foods can be consumed together or during the same eating episode (breakfast and snacks). To our knowledge, these 2 foods have never been studied in combination. In fact, common food combinations are rarely reported in the scientific literature. However, there are indications that consumption of certain foods may influence dietary intake of specific nutrients and food groups. For example, in the United States, in both sexes and across all age groups, consumption of ready-to-eat breakfast cereals was associated with higher intakes of milk and calcium ( 12 ). Similarly, in a cross-section of European adolescents (aged 12.5–17.5 years), consumption of ready-to-eat cereals was characterized by a better diet quality index, higher micronutrient intake, more frequent fruit consumption, and higher milk and yogurt consumption ( 13 ).

Dairy matrix and antioxidant enhancement of polyphenols

Not only can the intake of one food influence the consumption of another food, but there are also examples from in vitro and animal studies that the combination of certain nutrients has synergistic and/or complementary effects. An in vitro digestive model tested the antioxidant capacity of a green tea extract added to a matrix of dairy products (milk, yogurt or cheese) or a control.

Dairy matrix has been shown to enhance antioxidant activity by protecting the integrity of polyphenols during digestion ( 14 ). In an animal study, fermented milk containing yogurt cultures in addition to Bifidobacterium lactis CNCM I-2494 was more effective than pure B. lactis CNCM I-2494 strain in normalizing intestinal epithelial barrier junctions and reducing stress-induced visceral hypersensitivity in rats.

The efficacy of the fermented milk matrix compared to the pure probiotic strain has been attributed to the synergistic interactions between the probiotic strain, yogurt cultures, and metabolites in the fermented milk ( 15 ). Yogurt and fruits contain a wide variety of nutrients that have the potential to act in a complementary or synergistic manner on health. Whole fruit consumption has been recommended over supplement intake due to the synergistic activity of the bioactive components present in whole foods and their additive effects on health ( 16 ).

Dietary approaches that promote fruit and dairy mixtures

To manage hypertension, dietary approaches that promote fruit and vegetable mixes for their high potassium content and dairy products for their magnesium and calcium are recommended ( 17 ).

It is largely undisputed that fruits are protective against DRDs ( 18 ). These effects are mainly attributed to their high fiber content and antioxidant potential. There is increasingly strong evidence supporting yogurt consumption for its protective effect on specific DRDs, such as T2D ( 10 , 19 , 20 ) and obesity ( 2123 ). Mechanisms attributed to the potential health benefits of yogurt include its nutrient density, probiotic bacteria content, and fermented properties ( 24 , 25 ).

Potential synergistic and symbiotic impact

With the exception of specific supplements, foods and nutrients are rarely consumed in isolation; however, little is known or understood about food interactions in a dietary context. There is indeed a knowledge gap regarding the potential synergistic impact of food combinations, commonly identified in healthy dietary patterns, on health. This review will explore the potential for synergistic effects of yogurt and fruit consumption on DRDs, as well as their symbiotic potential as foods with probiotic and prebiotic properties. We hypothesized that consuming yogurt and fruit together could exert a synergistic effect on gut health, subsequently influencing DRDs.

Nutritional Profiles of Fruits and Yogurt

Fruits: nutrients, fiber, antioxidants and potential source of prebiotics.

Fruits are an excellent source of dietary fiber, potassium, antioxidants, phenolic compounds, and carotenoids (β-carotene, lycopene, lutein, and zeaxanthin) ( Figure 1 ), and have a very low energy density and high water content ( 26 , 27 ). Most fruits contain negligible amounts of fat and protein and little starch (with the exception of bananas) and have a relatively high proportion of simple sugars, such as fructose and sucrose ( 26 ). Fruits are particularly rich in insoluble fiber, which has the digestive benefit of adding bulk to the stool ( 26 ), and high-fiber diets have been linked to a lower incidence of gastrointestinal disease, cardiovascular disease (CVD), and some cancers ( 28 ).

Recommendations for fiber intake, established by the Institute of Medicine based on CVD risk, are rarely met in the United States ( 29 ). In a standard 2000 kcal/day diet, a single 100-g serving of fruit could provide between 7% and 53% of the recommended daily fiber intake (28 g/day) ( 30 ). High fiber intake protects against DRDs; the prebiotic properties of fruit are thought to contribute to its health-promoting potential ( 31 ). Fruits, vegetables, and grains are good sources of oligosaccharides, a dietary prebiotic fiber that promotes colonization of lactobacilli and bifidobacteria in the colon.

High consumption of fruits and vegetables may contribute ≤11.3 g of fructooligosaccharides to the human diet ( 32 ). Although specific prebiotic fibers have very interesting health benefits and can be isolated for use as functional additives in processed foods, it is the fiber in the original food matrix that may be responsible for conferring health benefits ( 31 ). Increasing fruit consumption would help deficient populations meet recommendations for dietary fiber intake.

Nutrients in yogurt and fruit that may impact the prevention of diet-related diseases alone and in combination.

Recommended daily servings of fruit

Recommendations for fruit and vegetable intake vary widely, but international recommendations are generally based on the 1997 joint World Cancer Research Fund/American Institute for Cancer Research report, which recommends five 80-g servings of fruit and vegetables, or 400 g/d ( 33 ).

Specific guidelines for fruit range from 1 to 5 servings/day in countries such as the United States, Australia, Germany, and China ( 2 ). It is known that specific cultivars, harvesting, storage, and preparation can result in variable amounts of phytonutrients among different fruits ( 27 ), potentially having variable health effects; however, health organizations have preferred to keep messages simple regarding consumption recommendations, comparing all fruits and vegetables. This partly reflects modern dietary habits with respect to availability and personal preferences, as well as epidemiological evidence, which rarely distinguishes between the quality or type of fruits and vegetables consumed. However, polyphenol-rich fruits have been extensively studied as the most potent health-promoting antioxidants in the human diet ( 34 ); berries and grapes are often separated from other fruits for this specific attribute ( 35 ). Berries in and of themselves, with their high polyphenol and antioxidant content, can be considered a naturally occurring functional health food ( 36 ). A polyphenol-rich extract of cranberry has recently been shown to exert anti-inflammatory properties, reduce weight gain, and improve several features of metabolic syndrome in high-fat-fed mice ( 37 ).

These effects have been linked to a significantly increased proportion of the mucin-degrading bacterium Akkermansia muciniphila in the gut microbiome of these mice. Similarly, the high polyphenol content of grapes has been shown to have beneficial effects on hypertension, T2D, CVD, cancer, and inflammation, among others ( 34 ), and a recent study confirmed that grape polyphenols may also protect against metabolic syndrome by increasing the proportion of A. muciniphila in the gut microbiome of mice ( 38 ).

Polyphenols have prebiotic activity

Given the ability of polyphenols to selectively stimulate the proliferation of beneficial microflora in the gut, it has been strongly suggested that polyphenols are endowed with prebiotic properties ( 39 ). Furthermore, polyphenolic compounds have been partly attributed to the beneficial effects of fruits on T2D ( 40 ). Fruit-rich diets contain prebiotic molecules (e.g., polyphenols), which have the ability to rebalance the microbial colonization of the gut, thus promoting metabolic health in the host ( 41 ). Overall, the nutrient density, fiber content, and prebiotic activity of fruits justify investments in public health nutrition promotion of increased fruit and vegetable intake as a strategy to reduce chronic diseases ( 18 ). However, specific recommendations on selecting fruits with a lower glycemic index may be advisable for individuals with T2D and those at risk of coronary artery disease (CAD) ( 42 ). Furthermore, fruit consumption may have a dose-response effect on T2D risk prevention and there may be no benefit beyond consumption of 2–3 (106 g) servings/day ( 11 ), which should be considered when providing balanced fruit and vegetable recommendations to the public.

Yogurt: Nutrient density and potential source of probiotics.

Traditional yogurt, defined as milk fermented with bacterial strains, is a source of probiotics that has established beneficial effects in vivo for lactose digestion. At present, however, it is unclear to what extent yogurt cultures have the ability to act as probiotics with respect to other health benefits ( 43 ). However, yogurt is a nutrient-dense, energy-packed food, containing between 0.2 and 3.8 g of fat, 3 and 6.5 g of protein, and 47 and 122 kcal per 100-g edible serving ( 44 ). It is an excellent source of calcium, vitamin D (in fortified yogurts), magnesium, vitamin B-12, and riboflavin ( Figure 1 ) ( 4547 ). It is also a good source of iodine for vulnerable populations in countries without an iodine-fortified food supply, such as the United Kingdom ( 48 ). The main carbohydrate in yogurt is lactose; However, its ability to be well tolerated by lactose-sensitive individuals is attributed to the presence of viable bacteria (e.g., Lactobacillus delbrueckii subspecies bulgaricus and Streptococcus thermophilus ) ( 49 ). In addition to containing lactose, many commercial yogurts contain sweeteners, making them a source of energy as well as a fair source of free sugars ( 45 ). However, sweetened yogurts may be a substantial source of added sugars only in very young children aged 4 months to 3 years, which likely reflects the limited diversity of the diet in this age group. Indeed, sweetened yogurts are not a substantial source of added sugars in older children and are an important source of key nutrients ( 45 ). The nutrient density of yogurt and its contribution to the intake of key nutrients is maintained despite the added sugar content of sweetened yogurts ( 50 ). As an excellent source of high-quality protein (from milk), many modern yogurts are further improved in protein concentration through manufacturing techniques and the addition of skim milk solids ( 51 ).

Commercial yogurts are available in a wide range of fat contents, including fat-free and low-fat varieties, which are foods promoted in nutritional guidelines as contributing to a balanced diet ( 47 ). Despite the popularity of fat-free yogurts, the presence of yogurt lipids has benefits that are often overlooked. Yogurt fat has important organoleptic properties; by maintaining a reasonable amount of fat in yogurt, a reduction in the amount of added sugars can be achieved while still keeping the yogurt palatable to consumers ( 21 ). The FA profile of yogurt is of particular interest, because it contains SCFA and medium-chain FA (10%), as well as CLA ( 52 ), which are thought to confer anticarcinogenic ( 53 ), anti-inflammatory ( 54 ), and antidiabetic ( 20 ) properties .

As a fermented product, yogurt has added health benefits over its primary ingredient, milk. Fermentation can increase the bioavailability of nutrients in yogurt, including vitamin B-12, calcium, and magnesium, among others, as well as proteins and peptides (especially in Greek yogurt), making it ideal for populations with frequent nutritional deficiencies and in children and the elderly, who need to build or maintain skeletal muscle mass ( 20 , 25 ). Active bacteria can act as probiotics, contributing to the microbial balance in the host's gastrointestinal tract when consumed in sufficient quantities ( 52 ). The viability of microorganisms in traditional yogurt remains controversial ( 55 ); however, it continues to be an important carrier for added probiotics known to have beneficial health effects. Bacterial fermentation of milk in yogurt alters the yogurt matrix, improving viscosity, osmolality, and energy density ( 56 ) and decreasing pH ( 57 ). The unique yogurt matrix results in a longer gastrointestinal transit time than milk, improving nutrient absorption and reducing gastrointestinal perturbations ( 58 ).

Both fruits and yogurt contain a huge variety of bioactive compounds, which can be enhanced or diminished during growth (ripening), storage, and processing. These small but sometimes significant differences make it very difficult to generalize results when comparing one type of food to all foods in the same category. Additionally, due to the complex nature of many foods and the fact that foods are not consumed in isolation, it is extremely difficult to ascertain whether potential health benefits are the result of specific foods or compounds within a given food.

Prebiotic, probiotic and symbiotic properties

Colonization of the gastrointestinal tract by microorganisms, known as the gut microbiota, creates an important barrier between the environment and the individual that protects against disease ( 59 ). The gut microbiota can be enhanced when probiotics, live, health-promoting organisms, are ingested in sufficient quantities to remain viable after passage through the gastrointestinal tract ( 60 ). On the other hand, prebiotics, which are dietary components, most often nondigestible carbohydrates, that induce the growth and activity of beneficial bacteria, provide a fermentable substrate for bacteria in the colon and remain insensitive to viability problems during digestion ( 61 ) . Prebiotics are 100% transferable to the colon, where they can be used to balance the microbiota, thereby providing beneficial systemic effects ( 62 ). Both prebiotics and probiotics play a role in modulating the microbiota ( 63 ). Research on probiotic foods has established the symbiotic effect of combining probiotic and prebiotic foods ( 59 ). Enhancement of the health benefits of the microbiota can be achieved with the use of synbiotics, defined by Gibson and Roberfroid ( 62 ) as “a mixture of probiotics and prebiotics that acts beneficially on the host by enhancing the survival and establishment of live microbial food supplements in the gastrointestinal tract, selectively stimulating the growth and/or activating the metabolism of one or a limited number of health-promoting bacteria” ( 62 ).

All species of the genus Lactobacillus are known to inhibit the growth of pathogenic bacteria, stimulate immune function and improve the bioavailability of food ingredients and minerals, including L. delbrueckii subspecies bulgaricus , typically used in traditional yogurt. Only some species of the genus Streptococcus , such as S. thermophilus , also present in traditional yogurt, are probiotic. In the book “The Prolongation of Life”, by Nobel Prize winner Elie Metchnikoff ( 64 ), yogurt containing lactobacilli was identified as being able to reduce pathogenic bacteria in the intestine, thus leading to increased longevity ( 65 ).

Probiotics are sensitive

However, Yogurt bacteria are sensitive to degradation during processing, as well as passage through the acidic environment of the stomach, and must be viable to be considered probiotic, generally requiring administration of 1–100 million CFU/g of food ( 66 ). Commercially produced yogurts generally provide adequate concentrations of probiotics in the range of 10 million to 10 billion CFU/g of food for a given 125- to 250-mL serving of yogurt ( 65 ). The advantage of consuming yogurt with fruit is the potential for prebiotics in fruit to help maintain the viability of probiotic bacteria in yogurt, as well as provide an additional substrate for increased activity once they reach the colon ( 62 , 67 ). Early prebiotic candidates contain fructooligosaccharides ( 62 ) and can be found in fruits such as bananas, nectarines, and raspberries ( 59 , 68 ). Furthermore, polyphenol-rich fruits may exert prebiotic effects, as highlighted by Anhê et al. ( 37 ); a polyphenol-rich cranberry extract administered to animals fed a high-fat, high-sugar diet resulted in a shift in the microbiota towards a marked increase in the relative abundance of Akkermansia ( 37 ).

In synbiotics, lactobacilli are commonly used as probiotic components ( 67 ), whereas oligosaccharides such as fructooligosaccharides are frequently used as prebiotic components ( 67 ). Synbiotics have largely been examined in the context of foods modified by the addition of functional probiotic and/or prebiotic ingredients ( 69 , 70 ) and not combinations of whole, minimally processed foods. The food matrix plays an important synergistic role in potentiating probiotics by demonstrating nutrients as well as a carrier for delivery to the gut ( 66 ), however food combinations with synbiotic properties have not been specifically examined.

Epidemiological Studies: Fruit, Yogurt, and Cardiometabolic Health

Food combinations such as yogurt and fruit have the potential to influence DRD prevention, particularly in developed countries, by offering nutritious ( Figure 1 ), energy-efficient alternatives to typical nutrient-poor snacks such as desserts and cookies ( 71 ). Some epidemiological evidence illustrates lower all-cause mortality in people who consume high amounts of fruit ( 72 ) and yogurt ( 73 ). Overall, there is strong support for the health benefits of fruit consumption in preventing chronic disease ( 18 ). Although there is a growing body of literature linking yogurt to health indicators, the case for yogurt in DRD is less well-established than that for fruit. However, increasing fruit and yogurt intake is among the strategies listed by Mozaffarian ( 74 ) as evidence-based key dietary priorities for cardiometabolic health. Furthermore, there is broad scientific consensus on the benefits of both fruit and yogurt with respect to cardiometabolic health ( 74 ). Taken together, dietary pattern analysis suggests that yogurt and fruit are common indicators of healthy dietary patterns that are protective against weight gain ( 75 ), T2D ( 76 ), and CVD ( 74 , 77 ).

Weight gain and obesity

Both yogurt and fruit have been identified as protective against weight gain ( 75 ). Results from the Framingham Heart Study Offspring Cohort (1991–2008) found that participants who consumed yogurt regularly (i.e., ≥3 times/wk) had lower annual weight gain and waist circumference gains than those who consumed <1 serving/wk ( 78 ). A review of yogurt and weight management examined 5 observational studies and found inconsistent results across studies regarding the association of yogurt with BMI, waist circumference, and sex ( 79 ). The Spanish Seguimiento University of Navarra (SUN) cohort was followed for an average of 6.6 years, and those with high intakes of whole and full-fat yogurt had a lower incidence of overweight or obesity. The inverse relationship between low-fat yogurt intake, risk of weight gain, and risk of overweight and obesity was only true for participants who also had a high fruit intake ( 80 ). Epidemiological studies indicate that there are significant associations between yogurt consumption and lower BMI, body weight, body weight gain, and body fat, and smaller waist circumference. However, well-designed randomized clinical trials have yet to provide evidence of a cause-effect relationship. ( 23 ).

Current findings suggest that increased intake of yogurt and fruit reduces intake of high-calorie foods ( 81 ). The influence of yogurt on weight gain may be attributed to changes in colonic bacteria due to ingestion of yogurt's abundant probiotics ( 75 ), whey, casein, and bioactive peptides ( 78 ). Yogurt consumption may increase the proportion of beneficial gut microbiota that is thought to be involved in weight maintenance through regulation of energy absorption and extraction ( 82 ). Furthermore, the high fiber content of fruit is assumed to increase satiety ( 75 ). Fruits are low in energy density and high in fiber and water, a combination that contributes to satiety and helps control weight ( 29 , 83 ). Despite expectations that high fruit and vegetable intake is inversely related to adiposity, the supporting evidence is weak ( 84 ). A systematic review and meta-analysis found only 2 studies that met all criteria and 5 other studies that met all criteria except one. The review found no association between fruit and vegetable intake and weight loss or obesity prevention among these 7 studies ( 85 ).

Type 2 Diabetes Mellitus (T2D)

In recent years, numerous studies have been conducted high-quality epidemiological studies and meta-analyses linking fruit and yogurt consumption to a lower incidence of T2D . A Spanish study that followed >3000 nondiabetic individuals for an average of 4.1 years found that total yogurt consumption was associated with a lower risk of T2D after multivariate adjustments for sociodemographic, lifestyle, and diet factors ( 20 ). This study also found a reduced risk of T2D after dietary modeling that replaced commonly consumed sweet snacks with a serving of yogurt. A British study involving 11 years of follow-up with a subsample of the European Prospective Investigation into Cancer and Nutrition-Norfolk study found a lower risk of type 2 diabetes with a high intake of low-fat fermented dairy products, primarily yogurt ( 19 ) . Similarly, A pooled analysis of 3 large US cohorts (Health Professionals Follow-Up Study, Nurses' Health Study, and Nurses' Health Study II) consistently showed an inverse association between yogurt and risk of T2D. ( 10 ). A meta-analysis including 7 yogurt studies investigated the association between dairy intake and T2D, revealing a marginally lower risk in the highest yogurt consumption group compared with the lowest amount consumption group ( 86 ). Chen et al. ( 10 ) updated this meta-analysis with 7 additional studies, including 3 large cohorts, and found that 1 serving of yogurt/d was associated with an 18% lower risk of incident T2D.

For fruit, the evidence for T2D risk has been less clear. A large prospective cross-European study involving 8 countries through the European Prospective Investigation into Cancer and Nutrition–InterAct found no significant associations between fruit intake and T2D risk ( 87 ). Similarly, this updated meta-analysis found no significant association between fruit intake and T2D risk. However, this analysis included only 5 studies, which found high heterogeneity, mainly attributed to differences in dietary measures ( 87 ). A subsequent meta-analysis of 10 studies found no heterogeneity for fruit and concluded that there was a significantly lower risk of T2D with high fruit intake ( 88 ). A recent meta-analysis investigating the dose-response of fruit and vegetable consumption found a nonlinear relationship between T2D and fruit intake, with the greatest risk reduction attributed to an intake of two to three 106 g/day servings ( 11 ). Given the strength of the current evidence, it would be reasonable to hypothesize that consumption of yogurt and fruit combinations could be beneficial for the prevention of T2D.

Cardiovascular Disease (CVD)

Among nutrition-related diseases (DRDs), cardiovascular disease is a major cause of morbidity worldwide, including in developing countries. It accounts for up to 23% of deaths and is the leading cause of death in the United States ( 89 ). Low fruit and vegetable consumption is a major risk factor for DRDs ( 90 ). It is believed that dietary interventions promoting increased fruit and vegetable consumption could lead to a significant decrease in CVD mortality ( 89 , 91 ).

The evidence for the protective effect of fruits and vegetables on cardiovascular health is particularly strong and consistent. The effects of fruits on CVD alone may, however, appear attenuated. Six prospective cohort studies were examined in a dose-response meta-analysis and found a borderline significant inverse association between CVD mortality and fruit consumption ( 72 ). A subsequent meta-analysis examining the association between fruit and vegetable consumption and CAD identified 15 studies with 25 dose-response ratios that compared low and high fruit intake and CAD risk. Of these studies, 6 reported strong inverse relationships; the pooled analysis revealed a 16% reduction in CAD risk associated with an intake of 300 g of fruit/day ( 91 ). Several attributes of fruit are attributed with heart-protective properties, including nutrient and phytochemical content (eg, fiber, potassium, and folate), low dietary glycemic load, and energy density ( 89 ).

Fruits high in polyphenols (e.g., berries, grapes) have additional heart-protective attributes through mechanisms that have the potential to reduce blood pressure, platelet activation, inflammation, oxidative stress, and LDL oxidation, while increasing endothelial function and the HDL-to-LDL ratio. ( 35 ).

Since dairy products appear to have a beneficial effect on CVD ( 92 ), yogurt has the potential to have similar effects. However, too few CVD studies have isolated yogurt consumption from total dairy consumption, making it difficult to draw conclusions. In a meta-analysis examining the relationship between dairy intake and risk of stroke, CAD, and CVD, no significant relationships were observed between yogurt consumption and stroke ( n = 3 studies) or CAD ( n = 5 studies). Similarly, with too few studies and no meta-analysis, the relationship between yogurt consumption and hypertension remains unclear with findings demonstrating positive ( 93 ), null ( 94 , 95 ), and inverse ( 96 , 97 ) relationships.

Challenges and future directions

Dietary combination data can be difficult to obtain, as common dietary data collection tools such as FFQs are generally not designed to capture this type of information. FFQs are often used because of their ease of application and low cost. The data generated by these tools are generally representative of predefined groups of food items and total daily nutrient intake. Although this type of dietary data collection is adequate for most study objectives, it is inflexible and may provide less information than repeated 24-hour recalls and food diaries, particularly with respect to eating episodes ( 98 ). Tools such as 24-hour dietary recalls and food diaries can capture meal-by-meal and snack-by-snack information, but dietary data analysis may not be conducted in a manner that allows for grouping of foods into specific eating episodes. These data collection tools were not designed to capture, enter, and collect information on food combinations. Although epidemiological studies have provided the best evidence linking dietary measures to health outcomes, they may not be the most appropriate for testing the concept of beneficial food combinations. The isolated effects of potential synbiotic food combinations (fruit and yogurt) on predetermined outcomes (glucose metabolism, FA metabolism, antioxidant profiles, and microbiota diversity) can be tested using carefully designed, placebo-controlled clinical trials.

Determinants of food choice are based on availability, sensory preferences, satiety, and social transmission ( 30 ). Fruits are widely available regardless of season or proximity to harvest; a wide variety of common and exotic fruits can be found in and out of season in Westernized countries ( 27 ). Both yogurt and fruit have a relatively low cost per pound compared to other animal-source foods ( 99 ). However, despite the widely available nature of fresh fruits, their affordability is still a barrier for some ( 100 ). Lifestyle factors are important contributors to dietary choices. Socially disadvantaged women tend to have lower fruit and yogurt consumption and lower-quality diets than their more privileged peers ( 101 ). In one study, active boys and girls consumed more fruit than their sedentary peers, and girls also consumed more yogurt ( 102 ). Inverse associations between yogurt and DRD have been hypothesized to be partially related to the likelihood that yogurt consumers lead healthier lifestyles ( 24 ). Public health agencies promote canned fruit over fresh fruit when accessibility or price are barriers; however, alarm has been raised about the appropriateness of these recommendations, given recent findings associating frequent consumption of canned fruit with cancer ( 103 ). Fruits are generally sweet and respond to innate taste preferences ( 26 ), likely making them more palatable than some vegetables. Although fruit has a low energy density, its fiber and water content give it satiating properties ( 83 ). Finally, fruit and yogurt are generally viewed positively ( 100 ), giving them a high potential for social transmission. According to the determinants of food choice, both fruit and yogurt would be selected and readily consumed by individuals with adequate means and accessibility. However, it is unclear whether current recommendations for fruits, vegetables, and dairy products are actually sustainable if the majority of the population began eating according to dietary guidelines ( 104 ).

Intake of fruits, vegetables, whole grains, dairy products, and seafood is suboptimal in the American diet, resulting in specific nutrients of concern: potassium, dietary fiber, calcium, and vitamin D ( 105 ). Regular consumption of yogurt and fruit in combination would help increase intake of all nutrients of concern, helping to fill nutrient gaps. Yogurt is a concentrated fermented milk, making it a nutrient-dense source of macro- and micronutrients, as well as a potentially high energy source. This is especially important when considering foods for populations vulnerable to malnutrition. For example, older adults often have suboptimal protein and energy intake, and yogurt is a valuable source of nutrients for this population in a concentrated format that is less expensive than most commercial nutritional supplements. Additionally, yogurt is an excellent source of vitamin D, calcium, and magnesium, nutrients important for maintaining bone health and preventing fractures in older adults ( 106 ). Specific dietary patterns that combine a variety of foods are known to be protective against DRDs. The prudent dietary pattern, which includes fruit and yogurt intake among its features, was strongly associated with a lower risk of both CVD and all-cause mortality ( 107 ). The Mediterranean diet, characterized in part by a high intake of fruits and vegetables and a moderate intake of dairy products, is known to have anti-cancer and anti-obesity properties ( 108 ).

Conclusion

To our knowledge, the symbiotic properties of food combinations such as yogurt and fruit have not been examined. Separately, both food groups are nutrient-dense and have demonstrated protective associations against DRD in epidemiological studies. There is reasonable evidence to suggest that, in combination, the probiotic properties of yogurt and the prebiotic properties of fruit are worthy of examination. In practice, foods are more often consumed in combination in meals and snacks than individually, and in countries where dairy products, fruit and vegetables are consumed in suboptimal amounts, interventions that promote combined intake of these food groups would be of value in encouraging consumption of healthy foods that are associated with both healthy dietary patterns and lifestyles. Given that public health nutrition has had limited success in increasing fruit and vegetable intake to optimal levels, marketing breakfast or snack combinations such as yogurt and fruit that require little preparation is a useful strategy for the prevention of DRD, particularly T2D. However, validation of the specific synergistic benefits of food combining is needed. Finding solutions to ensure that these specific food combinations are affordable and accessible year-round is particularly important for equitable prevention of DRD. Validation of the specific synergistic benefits of food combining is needed. Finding solutions to ensure that these specific food combinations are affordable and accessible year-round is particularly important for equitable prevention of DRD. Validation of the specific synergistic benefits of food combining is needed. Finding solutions to ensure that these specific food combinations are affordable and accessible year-round is particularly important for equitable prevention of DRD.


Sources:
  1. FAO. Food-based Dietary Guidelines [Internet]. 2015 [cited 4 July 2015]. Available at: http://www.fao.org/nutrition/nutrition-education/food-dietary-guidelines/en/ .
  2. Painter J, Rah JH, Lee YK. Comparison of pictorial representations of international food guides . J Am Diet Assoc 2002;102:483–9. [ PubMed ] [ Google Scholar ]
  3. Tuohy KM, Fava F, Viola R. “The road to a man’s heart is through his gut microbiota,” Dietary probiotics and prebiotics for cardiovascular risk management . Proc Nutr Soc 2014;73:172–85. [ PubMed ] [ Google Scholar ]
  4. Hong S, Song Y, Lee KH, Lee HS, Lee M, Jee SH, Joung H. A fruit- and dairy-based dietary pattern is associated with a reduced risk of metabolic syndrome . Metabolism 2012;61:883–90. [ PubMed ] [ Google Scholar ]
  5. Appel LJ, Moore TJ, Obarzanek E, Vollmer WM, Svetkey LP, Sacks FM, Bray GA, Vogt TM, Cutler JA, Windhauser MM, et al.. A clinical study of the effects of dietary patterns on blood pressure . N English J Med 1997;336:1117–24. [ PubMed ] [ Google Scholar ]
  6. Sacks FM, Svetkey LP, Vollmer WM, Appel LJ, Bray GA, Harsha D, Obarzanek E, Conlin PR, Miller ER, Simons-Morton DG, et al. Blood pressure effects of dietary sodium restriction and the diet for hypertension (DASH) diet-based approaches to stopping. N English J Med 2001;344:3–10. [ PubMed ] [ Google Scholar ]
  7. Hodge A, Bassett J. What can we learn from dietary pattern analysis? Public Health Nutr 2016; 19 :191–4. [ PubMed ] [ Google Scholar ]
  8. Hu FB. Dietary pattern analysis: a new direction in nutritional epidemiology . Curr Opin Lipidol 2002;13:3–9. [ PubMed ] [ Google Scholar ]
  9. Lecerf JM, Legrand P. Les effets des nutriments dépendent-ilsdes des aliments qui les portent? The matrix effect. [Do the effects of nutrients depend on the foods that contain them? The matrix effect.] Cahiers de nutrition et de diététique. 2015;50(3):158–64 (in French).
  10. Chen M, Sun Q, Giovannucci E, Mozaffarian D, Manson JE, Willett WC, Hu FB. Dairy intake and risk of type 2 diabetes: 3 cohorts of US adults and an updated meta-analysis . BMC Med 2014;12 :215. [ PMC free article ] [ PubMed ] [ Google Scholar ]
  11. Wu Y, Zhang D, Jiang X, Jiang W. Fruit and vegetable intake and risk of type 2 diabetes mellitus: a dose-response meta-analysis of prospective cohort studies. Nutr Metab Cardiovasc Dis 2015;25 :140–7. [ PubMed ] [ Google Scholar ]
  12. Song WO, Chun OK, Kerver J, Cho S, Chung CE, Chung SJ. Consumption of ready-to-eat breakfast cereals increases milk and calcium intake in the US population . J Am Diet Assoc 2006;106:1783–9. [ PubMed ] [ Google Scholar ]
  13. Michels N, De Henauw S, Breidenassel C, Censi L, Cuenca-García M, Gonzalez-Gross M, Gottrand F, Hallstrom L, Kafatos A, Kersting M, et al. European adolescent ready-to-eat cereals (RTEC) consumers have healthier dietary intake and body composition than non-RTEC consumers. Eur J Nutr 2015;54:653–64. Corrected and republished from: Eur J Nutr 2015;54:665–6. [ PMC free article ] [ PubMed ] [ Google Scholar ]
  14. Lamothe S, Azimy N, Bazinet L, Couillard C, Britten M. Interaction of green tea polyphenols with dairy matrices in a simulated gastrointestinal environment. Food Funct 2014; 5 :2621–31. [ PubMed ] [ Google Scholar ]
  15. Agostini S, Goubern M, Tondereau V, Salvador-Cartier C, Bezirard V, Lévèque M, Keränen H, Theodorou V, Bourdu-Naturel S, Goupil-Feuillerat N, et al.. A marketed fermented dairy product containing Bifidobacterium lactis CNCM I-2494 suppresses intestinal hypersensitivity and colonic barrier disruption induced by acute stress in rats. Neurogastroenterol Motil 2012;24 :376–e172. [ PubMed ] [ Google Scholar ]
  16. Liu RH. Health-promoting components of fruits and vegetables in the diet. Avv Nutr 2013;4 :384S–92S. [ PMC free article ] [ PubMed ] [ Google Scholar ]
  17. Most MM. Estimated phytochemical content of the Dietary Approaches to Stop Hypertension (DASH) diet is higher than that of the control study diet. J Am Diet Assoc 2004;104:1725–7. [ PubMed ] [ Google Scholar ]
  18. Boeing H, Bechthold A, Bub A, Ellinger S, Haller D, Kroke A, Leschik-Bonnet E, Muller MJ, Oberritter H, Schulze M, et al. Critical review: vegetables and fruits in the prevention of chronic diseases . Eur J Nutr 2012;51:637–63. [ PMC free article ] [ PubMed ] [ Google Scholar ]
  19. O'Connor LM, Lentjes M, Luben R, Khaw KT, Wareham N, Forouhi N. Dietary dairy product intake and incident type 2 diabetes: a prospective study using dietary data from a 7-day food diary. Diabetologia 2014;57:909–17. [ PMC free article ] [ PubMed ] [ Google Scholar ]
  20. Díaz-López A, Bullo M, Martínez-González MA, Corella D, Estruch R, Fito M, Gomez-Gracia E, Fiol M, Garcia de la Corte FJ, Ros E, et al. Dairy product consumption and risk of type 2 diabetes in an elderly Mediterranean Spanish population at high cardiovascular risk. Eur J Nutr 2016;55:349–60. [ PubMed ] [ Google Scholar ]
  21. Keast DR, Gallant KM, Albertson AM, Gugger CK, Holschuh NM. Associations between yogurt, dairy, calcium, and vitamin D intakes and obesity among US children aged 8 to 18 years: NHANES, 2005–2008. Nutrients 2015;7:1577–93. [ PMC free article ] [ PubMed ] [ Google Scholar ]
  22. Cormier H, Thifault É, Garneau V, Tremblay A, Drapeau V, Pérusse L, Vohl MC. Association between yogurt consumption, dietary patterns and cardiometabolic risk factors . Eur J Nutr 2016; 55 :577–87. [ PubMed ] [ Google Scholar ]
  23. Eales J, Lenoir-Wijnkoop I, King S, Wood H, Kok FJ, Shamir R, Prentice A, Edwards M, Glanville J, Atkinson RL. Is yogurt consumption associated with weight management outcomes? Results of a systematic review . Int J Obes (London) 2016;40 :731–46. [ PMC free article ] [ PubMed ] [ Google Scholar ]
  24. Wang H, Livingston KA, Fox CS, Meigs JB, Jacques PF. Yogurt consumption is associated with better diet quality and metabolic profile in American men and women. Nutr Res 2013;33:18–26. [ PMC free article ] [ PubMed ] [ Google Scholar ]
  25. Marette A, Picard-Deland E. Yogurt consumption and health impacts: focus on children and cardiometabolic risk . Am J Clin Nutr 2014;99:1243S–7S. [ PubMed ] [ Google Scholar ]
  26. Slavin JL, Lloyd B. Health benefits of fruits and vegetables . Avv Nutr 2012;3:506–16. [ PMC free article ] [ PubMed ] [ Google Scholar ]
  27. Terry LA. Health Benefits of Fruit and Vegetables . 1st ed Wallingford (UK): CABI; 2011. [ Google Scholar ]
  28. Padayachee A, Day L, Howell K, Gidley MJ. Complexity and health functionality of plant cell wall fibers from fruits and vegetables. Crit Rev Food Sci Nutr 2015. (Epub ahead of print; DOI: 10.1080/10408398.2013.850652). [ PubMed ] [ Google Scholar ]
  29. Slavin JL. Position of the American Dietetic Association: Health implications of dietary fiber . J Am Diet Assoc 2008;108:1716–31. [ PubMed ] [ Google Scholar ]
  30. Southgate DA. The nature and variability of human food consumption . Philos Trans R Soc Lond B Biol Sci 1991;334:281–8. [ PubMed ] [ Google Scholar ]
  31. Slavin J. Fiber and prebiotics: mechanisms and health benefits . Nutrients 2013;5:1417–35. [ PMC free article ] [ PubMed ] [ Google Scholar ]
  32. Delzenne NM. Oligosaccharides: state of the art. Proc Nutr Soc 2003;62:177–82. [ PubMed ] [ Google Scholar ]
  33. World Cancer Research Fund/American Cancer Institute. Nutrition, Diet, Physical Activity, and Cancer Prevention: A Global Perspective. Washington (DC) 1997. [ Google Scholar ]
  34. Rodriguez-Casado A. The health potential of fruit and vegetable pesticides: notable examples . Crit Rev Food Sci Nutr 2016; 56 :1097–107. [ PubMed ] [ Google Scholar ]
  35. Wightman JD, Heuberger RA. Effect of grapes and other berries on cardiovascular health . J Sci Food Agric 2015;95:1584–97. [ PubMed ] [ Google Scholar ]
  36. Szajdek A, Borowska EJ. Bioactive compounds and health properties of berries: a review. Plant Foods Hum Nutr 2008;63:147–56. [ PubMed ] [ Google Scholar ]
  37. Anhê FF, Roy D, Pilon G, Dudonne S, Matamoros S, Varin TV, Garofalo C, Moine Q, Desjardins Y, Levy E, et al. A polyphenol-rich cranberry extract protects against diet-induced obesity, insulin resistance, and intestinal inflammation in association with an increase in Akkermansia spp. population in the gut microbiota of mice. Gut 2015;64:872–83. [ PubMed ] [ Google Scholar ]
  38. Roopchand DE, Carmody RN, Kuhn P, Moskal K, Rojas-Silva P, Turnbaugh PJ, Raskin I. Dietary polyphenols promote growth of the gut bacterium Akkermansia muciniphila and attenuate high-fat diet-induced metabolic syndrome. Diabetes 2015;64:2847–58. [ PMC free article ] [ PubMed ] [ Google Scholar ]
  39. Neyrinck AM, Van Hee VF, Bindels LB, De Backer F, Cani PD, Delzenne NM. Polyphenol-rich extract of pomegranate peel alleviates tissue inflammation and hypercholesterolemia in high-fat diet-induced obese mice: potential implication of gut microbiota . Fr. J. Nutr 2013;109 :802–9. [ PubMed ] [ Google Scholar ]
  40. Anhê FF, Desjardins Y, Pilon G, Dudonné S, Genovese MI, Lajolo FM, Marette A. Polyphenols and type 2 diabetes: a prospective review. PharmaNutrition 2013; 1 :105–14. [ Google Scholar ]
  41. Anhê FF, Varin TV, Le Barz M, Desjardins Y, Levy E, Roy D, Marette A. Gut microbiota dysbiosis in obesity-related metabolic diseases and prebiotic potential of polyphenol-rich extracts . Rep. Curr Obes 2015;4 :389–400. [ PubMed ] [ Google Scholar ]
  42. Jenkins DJA, Srichaikul K, Kendall CWC, Sievenpiper JL, Abdulnour S, Mirrahimi A, Meneses C, Nishi S, He X, Lee S, et al.. The relationship between low-glycemic fruit consumption and glycemic control and risk factors for coronary heart disease in type 2 diabetes . Diabetologia 2011;54:271–9. [ PMC free article ] [ PubMed ] [ Google Scholar ]
  43. Guarner F, Perdigon G, Corthier G, Salminen S, Koletzko B, Morelli L. Should yogurt cultures be considered probiotics? Fr. J. Nutr 2005; 93 :783–6. [ PubMed ] [ Google Scholar ]
  44. Yildiz F. Development and production of yogurt and other functional dairy products. Boca Raton (FL): Taylor and Francis; 2010. [ Google Scholar ]
  45. Williams EB, Hooper B, Spiro A, Stanner S. The contribution of yogurt to nutrient intake across the lifespan . Nutr Bull 2015; 40 :9–32. [ Google Scholar ]
  46. Institute of Medicine. Dietary Reference Intakes for Calcium, Phosphorus, Magnesium, Vitamin D, and Fluoride . Washington (DC): National Academy Press; 1997. [ Google Scholar ]
  47. USDA National Nutrient Database for Standard Reference [Internet]. Agricultural Research Service, U.S. Department of Agriculture. 2014 [cited August 7, 2015]. Available from: http://ndb.nal.usda.gov/ .
  48. Pearce EN, Andersson M, Zimmermann MB. Global iodine nutrition: where are we in 2013? Thyroid 2013; 23 :523–8. [ PubMed ] [ Google Scholar ]
  49. Adolfsson O, Meydani SN, Russell RM. Yogurt and intestinal function . Am J Clin Nutr 2004; 80 :245–56. [ PubMed ] [ Google Scholar ]
  50. Nicklas TA, Drewnowski A, O'Neil CE. The nutrient density approach to healthy eating: challenges and opportunities . Public Health Nutr 2014;17:2626–36. [ PubMed ] [ Google Scholar ]
  51. Tamime AY, Robinson R. Yogurt: science and technology 3rd ed. Cambridge (UK): Woodhead Publishing; 2007. [ Google Scholar ]
  52. Chandan RC. Production of yogurt and fermented milks. 1st ed Ames, Iowa: Blackwell Publishing; 2006. [ Google Scholar ]
  53. Rodríguez-Alcalá LM, Fontecha J. Hot topic: fatty acid isomer composition and conjugated linoleic acid (CLA) of commercial dairy products fortified with CLA: evaluation after processing and storage. J Dairy Sci 2007;90:2083–90. [ PubMed ] [ Google Scholar ]
  54. Sofi F, Buccioni A, Cesari F, Gori A, Minieri S, Mannini L, Casini A, Gensini G, Abbate R, Antongiovanni M. Effects of a dairy product (pecorino) naturally rich in cis-9, trans-11 conjugated linoleic acid on lipid, inflammatory and hemorheological variables: a dietary intervention study. Nutr Metab Cardiovasc Dis 2010; 20 :117–24. [ PubMed ] [ Google Scholar ]
  55. Morelli L. Yogurt, living cultures and gut health . Am J Clin Nutr 2014;99:1248S–50S. [ PubMed ] [ Google Scholar ]
  56. Heaney RP. Excess dietary protein may not adversely affect bone . J Nutr 1998;128:1054–7. [ PubMed ] [ Google Scholar ]
  57. Savaiano DA. Digestion of lactose from yogurt: mechanism and relevance . Am J Clin Nutr 2014; 99 ( 5, Suppl )1251S–5S. [ PubMed ] [ Google Scholar ]
  58. Vonk RJ, Priebe MG, Koetse HA. Lactose intolerance: analysis of underlying factors. EUR J Clin Invest 2003;33:70–5. [ PubMed ] [ Google Scholar ]
  59. Galgano F, Condelli N, Caruso MC, Colangelo MA, Favati F. Probiotics and prebiotics in fruits and vegetables: technological and sensorial aspects . 1 ed In: Rai VR, Bai JA, editors. Beneficial microbes in fermented and functional foods . Boca Raton (FL): CRC Press-Taylor & Francis Group; 2015. [ Google Scholar ]

Related