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European Journal of Clinical Nutrition (2017) 71, 573–579

© 2017 Macmillan Publishers Limited, part of Springer Nature. All rights reserved 0954-3007/17
www.nature.com/ejcn

REVIEW
Yogurt, diet quality and lifestyle factors
S Panahi1, MA Fernandez2,3,4, A Marette2,4,5 and A Tremblay1,3,4

Yogurt consumption has been associated with healthy dietary patterns and lifestyles, better diet quality and healthier metabolic
profiles. Studies have shown that frequent yogurt consumers do not only have higher nutrient intakes, but also an improved diet
quality, which includes higher consumption of fruits and vegetables, whole grains, and dairy compared with low or non-consumers
indicating better compliance with dietary guidelines. Recent epidemiological and clinical evidence suggests that yogurt contributes
to better metabolic health because of its effects on the control of body weight, energy homeostasis and glycemic control.
Furthermore, yogurt consumers have been shown to be more physically active (⩾ 2 h/week), smoke less, have higher education
and knowledge of nutrition compared with non-consumers. Thus, yogurt consumption may be considered a signature of a healthy
diet through its nutritional content, impact on metabolic health including the control of energy balance, body weight and glycemia
and its relationships with healthier behaviors and lifestyle factors.

European Journal of Clinical Nutrition (2017) 71, 573–579; doi:10.1038/ejcn.2016.214; published online 2 November 2016

INTRODUCTION represent the overall combination of foods regularly consumed,


It is a matter of general belief that there are no detectable effects which collectively produce synergistic health effects.12 Growing
of a single food that could be sufficient enough to produce a evidence suggests that energy balance and metabolic regulation
change in the metabolic profile of individuals in a free-living are a consequence of multiple complex effects, particularly diet
context. However, recent studies have emphasized specific quality.12 Potential mechanisms for the control of energy balance
beneficial effects of yogurt consumption on body weight and and metabolism may include calorie-dependent and -indepen-
glycemic control.1–5 In a study examining the relationship dent effects of various types of foods on satiety, food intake,
between the effects of consumption of specific foods and long- glycemic response, visceral adiposity, brain reward systems,
term body weight changes, yogurt was found to predict a energy expenditure and the gut microbiome.13–17 Based on these
decrease in body weight over time.6 More recently, Chen et al.7 influences, when consumed over years, certain foods may
analyzed the relationship between dairy food consumption and promote a healthier body weight and contribute to improved
the proneness to type 2 diabetes in three large cohorts of men metabolic control.
and women. Although there were no associations between dairy Epidemiological studies suggest that dairy consumption is
consumption and the proneness to diabetes, a detailed analysis of linked to healthy dietary patterns, behaviors and lifestyle factors
specific dairy foods showed that yogurt consumption predicted a and is associated with a reduced risk for metabolic diseases
significantly lower risk of developing diabetes across the three including obesity and type 2 diabetes.8,18,19 Among the dairy
cohorts. In the same study, a meta-analysis of 14 prospective foods, yogurt has been of recent interest because of its high
cohorts showed a marginally lower risk of type 2 diabetes with nutrient density including the presence of calcium, magnesium
higher dairy consumption and a consistent inverse association and protein, lactic acid bacteria, which may affect gut microbiota
between yogurt consumption and type 2 diabetes risk.7 These and its ability to replace consumption of less healthy foods.20
observations are concordant with numerous population studies Short-term clinical trials of yogurt and its components have been
documenting the relationship between calcium and/or dairy shown to increase satiety, reduce food intake and improve
consumption and the predisposition towards glucose intolerance glycemic control.21–25 Dietary patterns such as the Meditteranean
and type 2 diabetes over time.8–11 Yogurt possesses unique and Dietary Approaches to Stop Hypertension recommend low-fat
physical and physiological properties that may impact body dairy products such as yogurt as part of a healthy diet, which may
weight and glycemic control. Furthermore, the relative energy and lead to an improvement in a range of risk factors for metabolic
nutrient content and contribution of yogurt to the overall diet diseases. After adjustment for the Nutrient-Rich Foods Index, a
suggest its nutrients largely contribute to nutrient requirements marker of diet quality, consumers of yogurt have been shown to
and provides a strong contribution to the regulation of energy have better anthropometric profiles, eating behaviors, physical
metabolism. However, it is also important to examine yogurt activity and metabolic health parameters that may help to prevent
consumption in the context of the overall diet. a positive energy balance compared with yogurt non-consumers
Healthy dietary patterns high in fruits and vegetables, low-fat (Panahi et al. unpublished data).
dairy, lean meats and pulses have been the cornerstone of obesity Several lifestyle factors also appear to interact with the diet and
prevention and diet-related chronic diseases. Dietary patterns its components to influence body weight and metabolic control

1
Department of Kinesiology, Université Laval, Québec City, Québec, Canada; 2Institute of Nutrition and Functional Foods, Université Laval, Québec City, Québec, Canada; 3School
of Nutrition, Université Laval, Québec City, Québec, Canada; 4Centre de Recherche de l`Institut de Cardiologie et de Pneumologie de Québec, Québec City, Québec, Canada and
5
Department of Medicine, Faculty of Agricultural and Food Sciences, Université Laval, Québec City, Québec, Canada. Correspondence: A Tremblay, Department of Kinesiology,
Université Laval, PEPS, Room 0234, 2300, rue de la Terrasse, Québec City, QC G1V 0A6, Canada.
E-mail: angelo.tremblay@kin.ulaval.ca
Received 24 May 2016; revised 19 September 2016; accepted 26 September 2016; published online 2 November 2016
Yogurt, diet and lifestyle
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including education, income, race/ethnicity, social norms and suggests that the % daily intake of these nutrients largely
network, local food availability, sleep quality and duration, contributes to nutrient requirements. In the absence of dairy
television viewing and physical activity.6,26,27 In some regions of consumption, it is difficult for individuals to meet the require-
the world, yogurt has been suggested to be a marker of an overall ments for several nutrients, particularly for North American diets.
healthy diet and thus, consumption is higher among those with a Dietary guidelines such as Canada’s Food Guide recommends
higher education19 and income.28 Thus, the question remains consumption of 2–4 servings of dairy products per day depending
whether the apparent improvements in health benefits are solely on age.33 Thus, taking into account the overall diet of each
attributed to yogurt consumption alone or whether the lifestyle individual, consuming at least one serving of yogurt per day may
factors have a role between yogurt consumers and non- help to increase the intake of many shortfall nutrients such as
consumers. Yogurt is readily available, accessible, a good source calcium, magnesium and potassium to meet dietary requirements.
of high-quality nutrients, simple to incorporate and a recom- In the National Health and Nutrition Examination Survey
mended component of the diet; however, few studies have (NHANES 2005–2008) investigating associations between yogurt
examined yogurt as part of a healthy dietary pattern and its and dairy consumption and energy, macronutrient and micro-
interaction with other lifestyle factors, which may affect the nutrient intakes in US children, yogurt consumers (defined as
metabolic profile of individuals (Figure 1). The potential role of consuming 41 serving of yogurt on one or both 24-h food recalls)
yogurt as a marker of a healthy diet and lifestyle will be described had higher intakes of calcium, vitamin D, protein and potassium
in this review by discussing the nutritional content of yogurt, its and lower intakes of total and saturated fats (% daily energy)
impact on cardiometabolic health (obesity and type 2 diabetes)
compared with non-consumers.31 Although greater dairy con-
and its relationship with sociodemographic and lifestyle factors.
sumption was associated with higher caloric and saturated fat
Furthermore, an overview of current gaps and future perspectives
intakes, yogurt consumption was not associated with higher
will be discussed.
energy intakes. This may have been due to the wide range of fat
contents found in dairy products such as cheese, ice cream and
YOGURT AND ITS NUTRITIONAL CONTENT fluid milk. Furthermore, the use of 24-h dietary recalls may not
Within the dairy products food group, yogurt is a nutrient-dense reflect habitual yogurt intakes, rely on memory and is susceptible
food with high digestibility, bioavailability of nutrients and to over and under-reporting. In a cross-sectional study examining
contains lactic acid bacteria, which may affect gut microbiota. It whether yogurt consumption was associated with better diet
is a complex mixture of proteins (whey protein and casein in the quality and metabolic profile among US adults (n = 6526)
ratio of 20:80), fats (saturated, mono- and poly-unsaturated fatty participating in the Framingham Heart Study Offspring (1998–
acids) and carbohydrate (lactose), providing high-quality nutrients, 2001) and Third Generation (2002–2005) cohorts, found that
which have a wide range of bioactivities.29 Although milk and yogurt consumers had higher potassium intakes and were 47%,
yogurt are similar in their nutrient composition, these unique 55%, 48%, 38% and 34% less likely to have inadequate intakes of
properties may provide additional health benefits. The nutritional vitamins B2, B12, calcium, magnesium and zinc, respectively
content of yogurt varies depending on the processing method (based on Dietary Reference Intakes).34 Another study, identifying
and ingredients used. Yogurt is distinct from other common fresh dietary insufficiencies and excesses in American children aged
dairy products as it is a by-product of milk fermentation, and 2–11, found that their diets consisted of extra energy, sugars and
contains live and active bacteria.30 Compared with milk, plain sodium but insufficient vitamin D, calcium and potassium. It was
yogurt is higher in specific nutrients including calcium, potassium suggested that substituting one serving of low sugar, whole milk
and protein as a result of the manufacturing and fermentation yogurt, paired with fruits or vegetables, for current snacks would
processes, which produce a more concentrated dairy product.31 increase children’s consumption of valuable nutrients without
As recently described in a review by Panahi and Tremblay32, the adding excess sugar or energy.35 Thus, consumption of yogurt
relative energy and nutrient content and contribution of a may improve nutrient adequacy and contribute to better overall
recommended serving of yogurt (175 g) to the overall diet diet quality.36,37

Figure 1. The potential relationship between yogurt consumption, diet and lifestyle factors.

European Journal of Clinical Nutrition (2017) 573 – 579 © 2017 Macmillan Publishers Limited, part of Springer Nature.
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YOGURT, DIETARY PATTERNS AND DIET QUALITY
Table 1. Differences between female yogurt consumers and non-
Dietary patterns are of importance as they consider multiple consumers for nutrients in which yogurt is not a primary source in the
aspects and dimensions of diet simultaneously (that is, total diet). Québec Family Studya
Rather than using the single food or nutrient approach, they have
the potential to capture interactions that may occur between Variable Yogurt consumption P-valueb
nutrients and other food components, which may help in the
development of dietary-based guidelines. One of the main Non-consumers Consumers
methods of assessing dietary patterns is the use of dietary indices (0 servings/day) ( ⩾ 1 servings/day)
or scores determined by a priori dietary guidelines and
Women
recommendations.38 Diet indices represent a measure of healthy N 62 21
eating patterns and are known as either diet quality or healthy Pantothenic acid (mg/day) 4.1 ± 1.7 5.5 ± 1.8 0.003
eating indices. The two most common diet scores include the Folic acid (mg/day) 167 ± 69 219 ± 81 0.01
Iron (mg/day) 14 ± 4 16 ± 6 0.03
Health Eating Index and Diet Quality Index based on the US Manganese (mg/day) 0.7 ± 0.6 1.5 ± 2.6 0.02
dietary guidelines; however, there are others including Mediterra- Copper (mg/day) 1.0 ± 0.8 1.2 ± 1.0 0.03
nean Diet Scores, Recommended Foods Score, Dietary Guidelines a
Adherence Index and Nutrient-Rich Foods Index.38,39 Some of Panahi et al.32 (unpublished data). bThe model was adjusted for age,
physical activity and % body fat. Data are means ± s.d.
these scores assess dietary quality on the basis of foods or food
groups, nutrients or combination of nutrients and foods. Although
using dietary scores have their limitations including the potential
lack of variation in population dietary intakes, and that few
individuals consume optimal diets (which may be a problem when account. In the INFOGENE study, yogurt consumption was found
assessing associations between diet and health outcomes), they to be a significant contributor to the Prudent dietary pattern,
indirectly assess intakes of nutrient and non-nutrient components which was also characterized by higher intakes of fruits and
in foods and contribute to food-based dietary guidelines. vegetables, nuts, non-hydrogenated fats, legumes, fish and other
Dietary guidelines for Americans suggest higher intakes of fat- seafood, whereas the Western dietary pattern was characterized
free and low-fat milk and milk products although this is currently by higher intakes of fried foods, certain condiments such as
debatable given that more studies are now demonstrating inverse sauces, ketchup or salt, processed meats, refined grains, snacks,
associations between consumption of higher fat dairy products red meats, high-fat dairy products such as ice cream, cream,
and cardiometabolic diseases such as obesity and type 2 regular soft drinks and alcohol.4
diabetes.40,41 Furthermore, Canada’s Food Guide recommends Consuming yogurt improves the overall nutritional quality of
consumption of 2–4 servings of dairy products per day depending the diet. Yogurt is suggested to be a major contributor of nutrients
on age. However, there are no recommendations for yogurt as a such as calcium; however, in the Québec Family Study, women
separate food item. Low-fat and fat-free yogurts represent a large who were consumers of yogurt (⩾ 1 servings/day) also had higher
proportion of the yogurt available and consumed in the United intakes of nutrients for which yogurt is generally not a rich source
States. They may be displacing other energy-dense foods or larger or a source at all including pantothenic acid, folic acid, copper,
portions in the diet or yogurt consumption may simply be a manganese and iron after adjustment for age, physical activity
marker for a more healthful dietary pattern. In US adults and % body fat (Table 1). Thus, yogurt consumers have a better
participating in the Framingham Heart Study Offspring (1998– intake of micronutrients even if yogurt is not a source of those
2001) and Third Generation (2002–2005) cohorts, yogurt con- nutrients.
sumers had a significantly higher Dietary Guidelines Adherence
Index score than non-consumers suggesting that consumers who
adhered to key dietary guidelines adherence recommendations YOGURT AND LIFESTYLE CHARACTERISTICS
were more likely to have a better overall diet quality.34 In a study Higher-quality diets including whole grains, lean meats, fish, low-
estimating the number of portions of different milk-based food fat dairy products and fresh fruits and vegetables have been
categories fitting into nutritionally adequate diets using individual associated with greater affluence, whereas energy-dense diets
diet modeling and data from adults in the 1999 French Enquête that are low in nutrients are consumed by individuals of lower
Individuelle et Nationale sur les Consommations Alimentaires socioeconomic status and more limited economic means.44
survey (n = 1171), it was found that across milk-based food Recent studies have documented various lifestyle characteristics
categories, the optimization of the diet increased yogurts (+60%) in yogurt consumers that have the potential to partly explain the
and milk (+17%) and decreased cheeses ( −48%) without a change reduced proneness to obesity and type 2 diabetes in these
to milk desserts.42 Cheeses represented one out of two consumed individuals including physical activity, smoking, level of education,
portions of milk-based products in observed diets, whereas in nutrition knowledge and socioeconomic status (Table 2).
modeled diets cheeses, milk and yogurts each represented about Yogurt consumption has been shown to be more common
one portion per day.42 Data from the NHANES (2003–2006) among healthier, leaner, more highly educated individuals from
assessed diet quality by the healthy eating index-2005 using one higher socioeconomic levels and more widespread among
24-h dietary recall and found that frequent yogurt consumers had women.45 Results from the INRAN-SCAI (2005–2006) survey on a
significantly better diet quality than infrequent consumers and sample of Italian households (n = 2798) showed that yogurt
consumed more fruits, whole grains and milk suggesting better consumers demonstrated healthier behaviors compared with
compliance to the recommendations of the dietary guidelines non-consumers.46 Higher intakes were reported by individuals
adherence.43 In many of these studies, the types of yogurt (for with higher levels of education, those practicing ⩾2 h of sporting
example, high-fat or low-fat, sweetened or unsweetened, plain, activities, those with a good knowledge of the food–health
probiotic) and quantities consumed were not assessed. However, relationship and accustomed to reading food labels.46 In a
for yogurt, the classication of 'high fat' versus 'low-fat' may be population-based cross-sectional health survey examining factors
arbitrary as the fat content remains low compared with other dairy associated with the probability and amounts of yogurt intake in
products such as hard cheeses or ice cream. Furthermore, other Brazilian adults and the elderly, higher yogurt intakes were
confounding factors such as physical activity, smoking, socio- positively associated with per capita family income and being a
economic and cultural considerations were not taken into non-smoker although level of education of the head of the

© 2017 Macmillan Publishers Limited, part of Springer Nature. European Journal of Clinical Nutrition (2017) 573 – 579
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Table 2. Relevant studies outlining lifestyle characteristics of yogurt consumers

Type N Diet quality Lifestyle factors Findings Study


indices used

Cross- 532 (428 adults NA Sociodemographic (sex, age, race, Yogurt intake associated with smoking Possa et al. 47
sectional aged 20–59 years education), economic (household (OR: 1.98), female sex (OR: 2.12), and
health and 104 elderly income) and lifestyle factors (smoking, age 20-39 years (OR: 3.11); Per capita
survey aged 460 years in physical activity, alcohol use), presence family income and being a non-
Brazil) of chronic conditions (hypertension, smoker were positively associated with
diabetes, osteoporosis), the amount of yogurt consumption
anthropometric (body weight, height) (coefficients, 0.61and 3.73)
Cross- 6526 (aged 5–70 DGAI score Age, physical activity, smoking Yogurt consumers smoked less Wang et al. 34
sectional years in United compared with non-consumers
States)
Cross- 2798 (aged 18–97 NA Sociodemographics, smoking and Yogurt intake associated with higher D`Addezio et al.46
sectional years in Italy) alcohol habits, physical activity, levels of education (P = 0.004), those
dieting, out-of-home eating, interest who practiced ⩾ 2 h/week of sporting
for nutrition information activities (P = 0.046), those with a good
knowledge of food–health relationship
(P = 0.012) and accustomed to reading
food labels (P = 0.002)
Cross- 5124 (aged 2–18 HEI score Sex, race, age, income-to-poverty ratio, Compared with infrequent consumers, Zhu et al.43
sectional years in United physical activity a higher percentage of frequent
States) yogurt consumers were Hispanic or
non-Hispanic whites, were younger
children aged 2–11 years, lived in
wealthier households and met the
physical activity recommendations (all
P o0.05)
Cross- 664 (aged 18–55Prudent Sex, education, matrimonial status, Consumers of yogurt were mainly Cormier et al.4
sectional years in Canada)
and personal income women (P = 0.008); Consumption of
Western yogurt was higher among those with a
Dietary university education and those who
Pattern were married/common-law, but not
score significant
Prospective 8516 (aged 18–101 NA Age, sex, physical activity, smoking, The highest category of total yogurt Martinez-
cohort years in Spain) years of university education, marital consumption (⩾7 servings per week) Gonzalez et al.18
status included a higher proportion of
women and participants were more
physically active (Po0.001), smoked
less (Po0.001) and were less likely to
be married (Po0.001)
Prospective 8063 (aged 18–101 NA Age, sex, physical activity, smoking, On average, participants in the highest Sayon-Orea et al.
64
cohort years in Spain) sitting time, TV watching, alcohol category of total yogurt consumption
consumption ( ⩾ 7 servings per week) were more
physically active (Po0.001), less likely
to be current smokers (Po 0.001),
spent less hours sitting (P = 0.06) and
consumed less alcohol (Po0.001)
Abbreviations: DGAI, Dietary Guidelines Adherence Index; HEI, Healthy Eating Index; NA, not applicable; OR, odds ratio.

household was inversely associated with yogurt intakes.47 sevenfold between 1974 and 2003.45 Currently, 40% of Brazilians
In addition, smokers had lower Health Eating Index scores as consume dairy products, but only 6% consume yogurt.45
evident from their lower consumption of fruits, vegetables and Yogurt consumers have been suggested to have better lifestyle
dairy products and diets high in sugar and fat compared with non- and eating behaviors that may help to prevent a positive energy
smokers. The socioeconomic factor of per capita family income balance and metabolic diseases compared with non-consumers. In
was positively associated with higher yogurt intakes as consump- the Québec Family Study comparing the profile of yogurt
tion in the group with the higher income is twice that the lower consumers and non-consumers in a cross-sectional sample of
income group. One of the potential factors limiting yogurt intake Québec men and women and over a mean follow-up of 6 years,
by populations with lower socioeconomic status is the perceived found that female yogurt consumers reported better dietary
high price of these products although some evidence suggests macronutrient composition, higher mean physical activity partici-
that yogurt possesses a reasonable cost to nutrient-density ratio.48 pation and better eating behaviors (that is, less disinhibition)
Furthermore, individuals with a higher socioeconomic status may compatible with body weight stability compared with non-
have greater knowledge of nutrition and be more concerned consumers when adjusted for age (Panahi et al., unpublished
about their health contributing to the positive association data). The benefits of regular yogurt consumption may have a
between amount of yogurt intake and household income. In wider influence on global healthy behaviors. These results
middle-income countries, yogurt consumption may be an complement other research findings demonstrating that yogurt
indicator of higher socioeconomic status. For example, although consumers are more physically active (⩾ 2 h/week) and 30% less
yogurt consumption in Brazil is low, it increased more than likely to smoke compared with non-consumers.47 Thus, the

European Journal of Clinical Nutrition (2017) 573 – 579 © 2017 Macmillan Publishers Limited, part of Springer Nature.
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lifestyle habits of yogurt consumers may predispose them to low-, moderate- or high-protein yogurt snacks on appetite control
better metabolic health not only because of the nutrient content and subsequent energy intake in healthy women (n = 15) found
of the food, but also due to the characteristics of other lifestyle that a yogurt snack with a high-protein content (24 g) reduced
factors. hunger, increased fullness and delayed the onset of eating
compared with lower protein snacks suggesting that a small, high-
protein afternoon snack regimen may delay or prevent subse-
YOGURT AND CARDIOMETABOLIC HEALTH quent snacking or over-eating later in the day.21 However, in this
Most research has included yogurt within a large category of dairy study it was unclear if the effects were attributed to the yogurt
products and few have examined yogurt as a separate food item itself or the functional protein that was added. A similar study
on overall health and metabolism. However, emerging research assessing the impact of protein composition and/or fiber
has demonstrated that yogurt may have positive effects on gut enrichment of consuming yogurt as a snack on appetite
microbiota,49,50 bone health,51 cardiovascular disease,52 type 2 sensations and energy intake in healthy men (n = 20) found that
diabetes7,11 and components of the metabolic syndrome such as although appetite sensations were not influenced by variations in
abdominal obesity.2,40,53 the protein composition or the fiber enrichment, a reduced
Epidemiological studies have shown that consuming dairy energy intake was observed during the ad libitum lunch after the
products such as milk and yogurt is associated with a beneficial high whey protein yogurt.58
role in metabolic regulation.8,18,19,54 In a prospective study of two
large cohorts, an increase in yogurt intake (1 serving/day) was
associated with a loss of 0.82 lb during a 4-year period.6 THE SUPPORT OF LABORATORY STANDARDIZED STUDIES
Furthermore, individuals with a habitual intake of 3 servings/ Even if there are some consistencies in the conclusions emerging
week had a smaller annual weight gain ( −0.10 ± 0.04 kg) than from epidemiological studies emphasizing benefits of yogurt
those consuming o 1 serving/week.34 In a cross-sectional study consumption, it remains relevant to rely on intervention studies
examining the relationship between diet quality and metabolic that demonstrate the causality between two variables. In this
profile in the Framingham Heart Study Offspring (1998–2001) and regard, physiological studies that have tested the acute effects of
Third Generation (2002–2005) cohorts, yogurt consumption (⩾1 yogurt consumption on energy intake, appetite sensations and
serving per week) was associated with lower concentrations of glycemia are worth considering. In a previously mentioned study
fasting glucose and insulin, homeostatic model assessment of in healthy men, yogurt with a higher content of whey protein
insulin resistance, systolic blood pressure, circulating triglycerides decreased subsequent ad libitum energy intake compared with
and better diet quality suggesting that yogurt is a good source of control yogurt formulation.58 Furthermore, high-protein afternoon
several macronutrients and micronutrients that may help to yogurt snacks (14 g protein/25 g carbohydrate/0 g fat) were also
maintain metabolic well being.34 However, observational studies found to increase satiety and reduce subsequent food intake in
have not been consistent. In many of these studies, the inverse healthy women compared with high-fat snacks such as crackers
associations between yogurt consumption and incidence of (0 g protein/19 g carbohydrate/9 g fat) and chocolate (2 g protein/
obesity and type 2 diabetes have been attributed to dietary 19 g carbohydrate/9 g fat).59 A study comparing isovolumetric
patterns. Furthermore, the wide range of composition in yogurt amounts (250 g) of plain yogurt, plain yogurt with honey,
products, including their protein and sugar contents, and variety strawberry yogurt, skim milk and orange juice as mid-morning
of yogurt products available have not been considered. Diverse snacks on food intake, satiety and pre- and post-meal blood
study populations, ethnicities and methods of intake measure- glucose and serum insulin in healthy males found that pre-meal
ment that do not measure habitual intake may also have glucose responses were attenuated in a dose-dependent manner
contributed to the inconsistent results. Furthermore, dietary to the increasing protein and decreasing sugars in dairy.22
patterns characterized by high intakes of yogurt and dairy However, the contribution of dairy products to post-meal glucose
products combined with higher intakes of whole grains, fruits control and to satiety and food intake was independent of their
and vegetables, are also negatively associated with the risk of protein to carbohydrate ratio and physical form in healthy men.22
weight gain and obesity54,55 and the incidence of type 2
diabetes.56,57 Epidemiological studies are primarily based on
subjective food recalls and in clinical studies, foods or food THE PRICE TO BE PAID FOR YOGURT CONSUMPTION
components are usually part of the diet. As a result, the role of Although it may be deemed reasonable to consider plain yogurt
yogurt and its potential physiologic mechanisms underlying the as the optimal formulation of this food, it is probably not the
observed effects cannot be isolated. Although many studies formulation that is the most attractive for consumers. This raises
demonstrate favorable associations between yogurt and body the question of the dilemma between palatability and function-
weight, differences in diet quality among countries and other ality of foods. Yogurt is perceived as a healthy food because of the
confounding factors such as physical activity, lifestyle, amount of presence of live and active cultures; however, artificial sweeteners,
yogurt consumption and other dietary factors need to be sugar and flavors are universally used by the food industry to
considered. Furthermore, for better elucidating the benefits of improve taste, attractiveness and acceptance by consumers.
yogurt, the dietary patterns and diet quality that are associated Yogurt manufacturers are working to decrease the amount of
with yogurt consumption should be taken into account. sugars in yogurt, but this raises an additional question as to what
Consuming dairy products such as yogurt has been associated is a reasonable compromise in yogurt sweetening to increase
with a beneficial role in metabolic regulation.8,18,19,54 Its nutrients palatability while maintaining its optimal functionality. In a study
have been shown to directly contribute to the nutrient density of comparing isovolumetric amounts (250 g) of plain yogurt, plain
the diet. Population studies have demonstrated that the diet yogurt with honey, strawberry yogurt, skim milk and orange juice
composition of yogurt consumers is characterized by an increased as mid-morning snacks on food intake, satiety, and glycemia,
intake of calcium, magnesium and protein, which have a critical strawberry yogurt was rated more palatable than plain yogurt.22
role in homeostasis. Although the number of long- and short-term However, no associations were found between palatability of the
randomized controlled trials is still modest, some clinical trials treatments, food intake and glycemia at the subsequent meal
have shown a beneficial effect of yogurt consumption on appetite suggesting that sweetening of yogurt improved palatability but
and glycemic control.21,58 Yogurt is also important because of its did not negatively affect glycemic response.
impact on concomitant energy intake and its influence on As high sugar intake has been associated with increased risk for
appetite and glycemic control. A study examining the effects of obesity and type 2 diabetes, there has been some concern about

© 2017 Macmillan Publishers Limited, part of Springer Nature. European Journal of Clinical Nutrition (2017) 573 – 579
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the addition of sugar to yogurt. However, previous studies Research Institute of the United States, Wyeth Consumer Healthcare and Nestlé.
examining various types of sugars on metabolic control have André Marette is a consultant for Danone Nutricia Research. Shirin Panahi and Angelo
shown that not all sugars are the same.60 Additional research is Tremblay have received an honorarium from Danone Nutricia Research.
required to further characterize the ideal concentration of sugar
that allows the optimal compromise between palatability and
functionality and a yogurt, which contains a minimum amount of ACKNOWLEDGEMENTS
added sugar. Furthermore, recent studies suggest that dairy fat The research of Angelo Tremblay is partly funded by the Canada Research Chair in
and full-fat dairy products may confer health benefits compared Environment and Energy Balance. André Marette’s research was partly funded by a
with non-fat or low-fat products.61,62 Choosing a whole milk CIHR/Pfizer Research Chair on the pathogenesis and cardiovascular diseases. Shirin
yogurt in place of a non-fat yogurt may also decrease the need for Panahi is the recipient of a postdoctoral fellowship from the Canadian Diabetes
added sugars to increase palatability, as the fat in yogurt provides Association.
flavor and increases satiety.35 Overall, it is important to emphasize
that moderation is a key component contributing to a healthy
dietary pattern and nutrition education may be one of the pillars REFERENCES
to decrease added sugar consumption.63 1 Diaz-Lopez A, Bullo M, Martinez-Gonzalez MA, Corella D, Estruch R, Fito M et al.
Dairy product consumption and risk of type 2 diabetes in an elderly Spanish
Mediterranean population at high cardiovascular risk. Eur J Nutr 2016; 55:
FUTURE PERSPECTIVES 349–360.
2 Babio N, Becerra-Tomas N, Martinez-Gonzalez MA, Corella D, Estruch R, Ros E et al.
Given the relatively low yogurt consumption in various countries, Consumption of yogurt, low-fat milk, and other low-fat dairy products is asso-
increasing yogurt intake may be promising in helping to achieve ciated with lower risk of metabolic syndrome incidence in an elderly Mediterra-
greater adequacy for some of the shortfall nutrients and maintain nean population. J Nutr 2015; 145: 2308–2316.
metabolic well-being as part of a healthy, energy-balanced dietary 3 O'Connor L, Lentjes M, Luben R, Khaw K, Wareham N, Forouhi NG. Dietary dairy
pattern. Low consumption of yogurt may represent a missed product intake and incident type 2 diabetes: a prospective study using dietary
opportunity to contribute to healthy eating habits, as yogurt data from a 7- day food diary. Diabetologia 2014; 57: 909–917.
provides an excellent source of highly bioavailable protein and 4 Cormier H, Thifault É, Garneau V, Tremblay A, Drapeau V, Pérusse L et al. Asso-
calcium and is a source of probiotics that are believed to provide a ciation between yogurt consumption, dietary patterns, and cardio-metabolic risk
range of health benefits. factors. Eur J Nutr 2015; 55: 577–587.
5 Moreno LA, Bel-Serrat S, Santaliestra-Pasias A, Bueno G. Dairy products, yogurt
Observational studies examining the effect of yogurt as part of a
consumption, and cardiometabolic risk in children and adolescents. Nutr Rev
healthy diet and yogurt and various health outcomes exist; 2015; 73(Suppl 1): 8–14.
however, there are some factors to consider. It is important to 6 Mozaffarian D, Hao T, Rimm EB, Willett WC, Hu FB. Changes in diet and lifestyle
better control for differences in diet and lifestyle. For example, and long-term weight gain in women and men. N Engl J Med 2011; 364:
confounding factors including physical activity, lifestyle habits 2392–2404.
such as smoking and alcohol and yogurt intake levels need to be 7 Chen M, Sun Q, Giovannucci E, Mozaffarian D, Manson JE, Willett WC et al. Dairy
considered. Population studies in which appropriate adjustments consumption and risk of type 2 diabetes: 3 cohorts of US adults and an updated
can be performed for diet quality and food-related behaviors as meta-analysis. BMC Med 2014; 12: 215.
potential factors observed between consumers and non- 8 Aune D, Norat T, Romundstad P, Vatten LJ. Dairy products and the risk of type 2
consumers of yogurt are needed. Furthermore, as is the case diabetes: a systematic review and dose-response meta-analysis of cohort studies.
Am J Clin Nutr 2013; 98: 1066–1083.
with many other functional foods, it is important to examine
9 Gao D, Ning N, Wang C, Wang Y, Li Q, Meng Z et al. Dairy products consumption
whether the benefits of yogurt are a result of its independent and risk of type 2 diabetes: systematic review and dose-response meta-analysis.
effects or whether other factors have a role. Thus, long-term PLoS One 2013; 8: e73965.
clinical trials need to be designed to provide a more realistic 10 Kirii K, Mizoue T, Iso H, Takahashi Y, Kato M, Inoue M et al. Calcium, vitamin D and
assessment of yogurt's health benefits and that are ecologically dairy intake in relation to type 2 diabetes risk in a Japanese cohort. Diabetologia
valid and will lead to dietary recommendations. There is also a lack 2009; 52: 2542–2550.
of studies examining yogurt types including low-fat, full-fat, plain, 11 Tong X, Dong JY, Wu ZW, Li W, Qin LQ. Dairy consumption and risk of type 2
fruit, Greek and probiotic- and sugar-containing yogurts. Future diabetes mellitus: a meta-analysis of cohort studies. Eur J Clin Nutr 2011; 65:
studies should consider the overall diet and its composition since 1027–1031.
many studies have considered energy, type and amount of yogurt, 12 Mozaffarian D. Dietary and policy priorities for cardiovascular disease, diabetes,
and obesity: a comprehensive review. Circulation 2016; 133: 187–225.
timing (for example, snack, part of a meal) and frequency of
13 Ludwig DS, Friedman MI. Increasing adiposity: consequence or cause of over-
consumption as factors. It is also important to target populations eating? JAMA 2014; 311: 2167–2168.
with a high risk for metabolic diseases including individuals with 14 Ebbeling CB, Swain JF, Feldman HA, Wong WW, Hachey DL, Garcia-Lago E et al.
obesity, type 2 diabetes or cardiovascular disease. Studies should Effects of dietary composition on energy expenditure during weight-loss main-
also include children and older adults to assess differences in the tenance. JAMA 2012; 307: 2627–2634.
contribution of yogurt to various health outcomes including body 15 Lennerz BS, Alsop DC, Holsen LM, Stern E, Rojas R, Ebbeling CB et al. Effects of
weight and glycemic control among these age groups. dietary glycemic index on brain regions related to reward and craving in men. Am
J Clin Nutr 2013; 98: 641–647.
16 Panahi S, El Khoury D, Luhovyy BL, Goff HD, Anderson GH. Caloric beverages
CONCLUSION consumed freely at meal-time add calories to an ad libitum meal. Appetite 2013;
Yogurt consumption may be considered a signature of a healthy 65: 75–82.
17 Panahi S, Luhovyy BL, Liu TT, Akhavan T, El Khoury D, Goff HD et al. Energy and
diet through its nutritional content, impact on metabolic health
macronutrient content of familiar beverages interact with pre-meal intervals to
including the regulation of energy balance, body weight and determine later food intake, appetite and glycemic response in young adults.
glycemia and its relationships with healthier behaviors and Appetite 2013; 60: 154–161.
lifestyle factors. 18 Martinez-Gonzalez MA, Sayon-Orea C, Ruiz-Canela M, de la Fuente C,
Gea A, Bes-Rastrollo M. Yogurt consumption, weight change and risk of over-
weight/obesity: the SUN cohort study. Nutr Metabol Cardio Dis 2014; 24:
CONFLICT OF INTEREST 1189–1196.
Angelo Tremblay serves on the Yogurt in Nutrition Initiative for Health Advisory 19 Vergnaud AC, Peneau S, Chat-Yung S, Kesse E, Czernichow S, Galan P et al. Dairy
Board for Danone Institute International and on the board of the Danone Institute of consumption and 6-y changes in body weight and waist circumference in middle-
Canada. His research has been funded, in part, by Dairy Farmers of Canada, the Dairy aged French adults. Am J Clin Nutr 2008; 88: 1248–1255.

European Journal of Clinical Nutrition (2017) 573 – 579 © 2017 Macmillan Publishers Limited, part of Springer Nature.
Yogurt, diet and lifestyle
S Panahi et al
579
20 Tremblay A, Doyon C, Sanchez M. Impact of yogurt on appetite control, energy 44 Darmon N, Drewnowski A. Does social class predict diet quality? Am J Clin Nutr
balance, and body composition. Nutr Rev 2015; 73(Suppl 1): 23–27. 2008; 87: 1107–1117.
21 Douglas SM, Ortinau LC, Hoertel HA, Leidy HJ. Low, moderate, or high protein 45 Fisberg M, Machado R. History of yogurt and current patterns of consumption.
yogurt snacks on appetite control and subsequent eating in healthy women. Nutr Rev 2015; 73(Suppl 1): 4–7.
Appetite 2013; 60: 117–122. 46 D`Addezio L, Mistura L, Sette S, Turrini A. Sociodemographic and lifestyle char-
22 El Khoury D, Brown P, Smith G, Berengut S, Panahi S, Kubant R et al. Increasing the acteristics of yogurt consumers in Italy: results from the INRAN-SCAI 2005-
protein to carbohydrate ratio in yogurts consumed as a snack reduces post- 06 survey. Medit J Nutr Metabol 2015; 8: 119–129.
consumption glycemia independent of insulin. Clin Nutr 2014; 33: 29–38.
47 Possa G, de Castro MA, Marchioni DM, Fisberg RM, Fisberg M. Probability and
23 Panahi S, El Khoury D, Kubant R, Akhavan T, Luhovyy BL, Goff HD et al. Mechanism
amounts of yogurt intake are differently affected by sociodemographic, eco-
of action of whole milk and its components on glycemic control in healthy
nomic, and lifestyle factors in adults and the elderly-results from a population-
young men. J Nutr Biochem 2014; 25: 1124–1131.
based study. Nutr Res 2015; 35: 700–706.
24 Akhavan T, Luhovyy BL, Brown PH, Cho CE, Anderson GH. Effect of premeal
48 Darmon N, Drewnowski A. Contribution of food prices and diet cost to socio-
consumption of whey protein and its hydrolysate on food intake and postmeal
economic disparities in diet quality and health: a systematic review and analysis.
glycemia and insulin responses in young adults. Am J Clin Nutr 2010; 91: 966–975.
25 Akhavan T, Luhovyy BL, Panahi S, Kubant R, Brown PH, Anderson GH. Mechanism Nutr Rev 2015; 73: 643–660.
of action of pre-meal consumption of whey protein on glycemic control in 49 Garcia-Albiach R, Pozuelo de Felipe MJ, Angulo S, Morosini MI, Bravo D, Baquero F
young adults. J Nutr Biochem 2014; 25: 36–43. et al. Molecular analysis of yogurt containing Lactobacillus delbrueckii subsp.
26 Mozaffarian D, Afshin A, Benowitz NL, Bittner V, Daniels SR, Franch HA et al. bulgaricus and Streptococcus thermophilus in human intestinal microbiota. Am
Population approaches to improve diet, physical activity, and smoking habits: a J Clin Nutr 2008; 87: 91–96.
scientific statement from the American Heart Association. Circulation 2012; 126: 50 Zhong Y, Huang CY, He T, Harmsen HM. [Effect of probiotics and yogurt on
1514–1563. colonic microflora in subjects with lactose intolerance]. Wei Sheng Yan Jiu
27 Christakis NA, Fowler JH. The spread of obesity in a large social network over J Hygiene Res 2006; 35: 587–591.
32 years. N Engl J Med 2007; 357: 370–379. 51 Sahni S, Tucker KL, Kiel DP, Quach L, Casey VA, Hannan MT. Milk and yogurt
28 Allen S, Goddard E. Consumer preferences for milk and yogurt attributes: How consumption are linked with higher bone mineral density but not with hip
health beliefs and attitudes affect choices. 2012; 1-45. Available from http://age fracture: the Framingham Offspring Study. Arch Osteo 2013; 8: 119.
consearch.umn.edu/bitstream/125012/2/Allen.pdf. 52 Ralston RA, Lee JH, Truby H, Palermo CE, Walker KZ. A systematic review and
29 Ebringer L, Ferencik M, Krajcovic J. Beneficial health effects of milk and fermented meta-analysis of elevated blood pressure and consumption of dairy foods.
dairy products - review. Folia Microbiol (Praha) 2008; 53: 378–394. J Human Hyperten 2012; 26: 3–13.
30 Marette A, Picard-Deland E. Yogurt consumption and impact on health: focus on 53 Beydoun MA, Gary TL, Caballero BH, Lawrence RS, Cheskin LJ, Wang YF. Ethnic
children and cardiometabolic risk. Am J Clin Nutr 2014; 99(5 Suppl): differences in dairy and related nutrient consumption among US adults and their
1243S–1247SS. association with obesity, central obesity, and the metabolic syndrome. Am J Clin
31 Keast DR, Hill Gallant KM, Albertson AM, Gugger CK, Holschuh NM. Associations
Nutr 2008; 87: 1914–1925.
between yogurt, dairy, calcium, and vitamin D intake and obesity among US
54 Pereira MA, Jacobs Jr DR, Van Horn L, Slattery ML, Kartashov AI, Ludwig DS. Dairy
children aged 8-18 years: NHANES, 2005-2008. Nutrients 2015; 7: 1577–1593.
consumption, obesity, and the insulin resistance syndrome in young adults: the
32 Panahi S, Tremblay A. The potential role of yogurt in weight management and
CARDIA Study. JAMA 2002; 287: 2081–2089.
prevention of type 2 diabetes. J Am Coll Nutr 2016; 22: 1–15.
33 Health Canada. Eating well with Canada`s Food Guide 2007. Available from http:// 55 Drapeau V, Despres JP, Bouchard C, Allard L, Fournier G, Leblanc C et al. Mod-
www.hc-sc.gc.ca/fn-an/food-guide-aliment/index-eng.php. ifications in food-group consumption are related to long-term body-weight
34 Wang H, Livingston K, Fox C, Meigs J, Jacques P. Yogurt consumption is associated changes. Am J Clin Nutr 2004; 80: 29–37.
with better diet quality and metabolic profile in American men and women. Nutr 56 Erber E, Hopping BN, Grandinetti A, Park SY, Kolonel LN, Maskarinec G. Dietary
Res 2013; 33: 18–26. patterns and risk for diabetes: the multiethnic cohort. Diabetes Care 2010; 33:
35 Hess J, Slavin J. Snacking for a cause: nutritional insufficiencies and excesses of US 532–538.
children, a critical review of food consumption patterns and macronutrient and 57 Villegas R, Yang G, Gao YT, Cai H, Li HL, Zheng W et al. Dietary patterns are
micronutrient intake of U.S. children. Nutrients 2014; 6: 4750–4759. associated with lower incidence of type 2 diabetes in middle-aged women: the
36 Ranganathan R, Nicklas TA, Yang SJ, Berenson GS. The nutritional impact of dairy Shanghai Women's Health Study. Int J Epidemiol 2010; 39: 889–899.
product consumption on dietary intakes of adults (1995-1996): the Bogalusa 58 Doyon CY, Tremblay A, Rioux LE, Rheaume C, Cianflone K, Poursharifi P et al. Acute
Heart Study. J Am Diet Assoc 2005; 105: 1391–1400. effects of protein composition and fibre enrichment of yogurt consumed as
37 Weinberg LG, Berner LA, Groves JE. Nutrient contributions of dairy foods in the snacks on appetite sensations and subsequent ad libitum energy intake in
United States, Continuing Survey of Food Intakes by Individuals, 1994-1996, 1998. healthy men. Appl Physiol Nutr Metab 2015; 40: 980–989.
J Am Diet Assoc 2004; 104: 895–902. 59 Ortinau LC, Hoertel HA, Douglas SM, Leidy HJ. Effects of high-protein vs. high- fat
38 McNaughton SA, Ball K, Crawford D, Mishra GD. An index of diet and eating patterns snacks on appetite control, satiety, and eating initiation in healthy women. Nutr J
is a valid measure of diet quality in an Australian population. J Nutr 2008; 138: 86–93. 2014; 13: 97.
39 Mistura L, D'Addezio L, Sette S, Piccinelli R, Turrini A. Diet quality of Italian yogurt
60 St-Pierre P, Pilon G, Dumais V, Dion C, Dubois M, Dubé P et al. Comparative
consumers: an application of the probability of adequate nutrient intake score
analysis of maple syrup to other natural sweeteners and evaluation of their
(PANDiet). Int J Food Sci Nutr 2016; 67: 232–238.
metabolic responses in healthy rats. J Func Foods II 2014; 11: 460–471.
40 Drehmer M, Pereira MA, Schmidt MI, Alvim S, Lotufo PA, Luft VC et al. Total and
61 Kratz M, Baars T, Guyenet S. The relationship between high-fat dairy consumption
full-fat, but not low-fat, dairy product intakes are inversely associated with
and obesity, cardiovascular, and metabolic disease. Eur J Nutr 2013; 52: 1–24.
metabolic syndrome in adults. J Nutr 2016; 146: 81–89.
41 Nestel PJ, Mellett N, Pally S, Wong G, Barlow CK, Croft K et al. Effects of low-fat or 62 Holmberg S, Thelin A. High dairy fat intake related to less central obesity: a male
full-fat fermented and non-fermented dairy foods on selected cardiovascular cohort study with 12 years' follow-up. Scand J Prim Health Care 2013; 31: 89–94.
biomarkers in overweight adults. Br J Nutr 2013; 110: 2242–2249. 63 Saint-Eve A, Oettgen W, Leclercq H, Delarue J, Berthelo S, Saulnier B. How much
42 Clerfeuille E, Maillot M, Verger EO, Lluch A, Darmon N, Rolf-Pedersen N. Dairy products: sugar do consumers add to plain yogurts? Insights from a study examining
how they fit in nutritionally adequate diets. J Acad Nutr Diet 2013; 113: 950–956. French consumer behavior and self-reported habits. Appetite 2016; 99: 277–284.
43 Zhu Y, Wang H, Hollis JH, Jacques PF. The associations between yogurt con- 64 Sayon-Orea C, Bes-Rastrollo M, Marti A, Pimenta AM, Martin-Calvo N, Martinez-
sumption, diet quality, and metabolic profiles in children in the USA. Eur J Nutr Gonzalez MA. Association between yogurt consumption and the risk of metabolic
2015; 54: 543–550. syndrome over 6 years in the SUN study. BMC Public Health 2015; 15: 170.

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