Moore, 2018
Moore, 2018
BMJ Open: first published as 10.1136/bmjopen-2017-021387 on 18 September 2018. Downloaded from http://bmjopen.bmj.com/ on 29 November 2018 by guest. Protected by copyright.
                                        Evaluation of the nutrient content of
                                        yogurts: a comprehensive survey of
                                        yogurt products in the major
                                        UK supermarkets
                                        J Bernadette Moore,1,2 Annabelle Horti,1 Barbara A Fielding2
                                                                                                                                                BMJ Open: first published as 10.1136/bmjopen-2017-021387 on 18 September 2018. Downloaded from http://bmjopen.bmj.com/ on 29 November 2018 by guest. Protected by copyright.
associated with lower risk of obesity and cardiometabolic
                                                                   Table 1  Definitions
risk in both children and adults.6 7
   Evidence is accumulating that frequent yogurt                   Term               Definition
consumption may be associated with healthier meta-                 Sugars*            Conventionally describes chemically the
bolic profiles in both children and adults.8 9 In adults,                             monosaccharides (glucose, fructose,
increased yogurt consumption has been associated with                                 galactose) and disaccharides (sucrose,
lower levels of circulating triglycerides, glucose and lower                          lactose†, maltose).
systolic blood pressure9; and several recent meta-analyses         Total sugars       Currently required for UK nutrition label.
have demonstrated that increased yogurt consumption                                   Includes sugars occurring naturally in foods
is inversely associated with the risk of developing type 2                            and beverages and those added during
                                                                                      processing and preparation.
diabetes (T2D).10–13 Notably, across three large American
cohort studies (the Health Professionals Follow-Up Study           Free sugars  ‘All monosaccharides and disaccharides
and the Nurses’ Health Studies I and II) in >190 000 adults                     added to foods by the manufacturer, cook
                                                                                or consumer, plus sugars naturally present
and >30 years of follow-up, while there was no effect of
                                                                                in honey, syrups and unsweetened fruit
dairy on incident T2D, yogurt intake specifically was                           juices. Under this definition lactose† when
inversely associated with T2D risk across the three cohorts                     naturally present in milk and milk products
with a pooled HR of 0.83 (0.75, 0.92) for one serving/                          is excluded.’36 Sugars present in intact fruits
day.12 Although confounders were statistically accounted                        and vegetables are also excluded.
for, an acknowledged limitation to these epidemiology              Added sugars ‘Syrups and other caloric sweeteners used
studies is the evidence that yogurt is a general marker                         as a sweetener in other food products.
of healthy dietary habits.9 14 Data are more equivocal                          Naturally occurring sugars such as those
regarding yogurt consumption and cardiovascular disease                         in fruit or milk are not added sugars.’61 In
risk, although one study suggested a possible lowered                           addition, excludes sugars in juiced or pureed
risk at higher levels of yogurt intakes (>200 g/day),15 a                       fruits and vegetables that are included in
                                                                                definition of free sugars. Will be a required
more recent and comprehensive meta-analysis showed
                                                                                subline under ‘total sugars’ for US food
no benefit.16 High-quality and adequately powered                               labels from 2020.46
randomised controlled trials are lacking however.
   Prospective cohort studies have, in general, shown              Adapted with permission from Moore and Fielding [34].
                                                                   *Examples of sugars commonly found as ingredients: sucrose,
inverse associations between yogurt intakes and changes
                                                                   fructose, glucose, dextrose, maltose, lactose, trehalose, brown
in waist circumference, weight and risk of overweight or           sugar, turbinado sugar, demerara sugar, raw sugar, cane sugar, fruit
obesity; with some inconsistencies between studies.17 18           sugar, invert sugar, corn sweetener, corn syrup, high-fructose corn
More recently, in an elderly Italian population cohort             syrup, malt syrup, glucose syrup, glucose-fructose syrup, fructose-
of >4000 at high cardiovascular risk, consumption of               glucose syrup, honey, molasses, date syrup, agave syrup.
                                                                   †Lactose is often called ‘milk sugar’ because 100% of ‘total
whole-fat yogurt (but not total yogurt) was associated
                                                                   sugars’ in milk are lactose. In natural/Greek yogurt ~80% of the
with changes in waist circumference and higher proba-              sugar is lactose, with the remainder being galactose generated
bility for reversion of abdominal obesity and lower risk of        from lactose fermentation.62
diabetes.19 20 This is in line with a previous systematic review
of observational studies on the relationship between dairy
fat, obesity and cardiometabolic disease; in 11 of 16 studies        In the UK, on average, children consume more
included in the review, high-fat dairy intake was inversely        yogurt than adults, and children under 3 years of age
associated with measures of adiposity.21 While dietary             have the highest intakes.27 Yogurt contributes a signifi-
guidelines vary by region, most countries make dietary             cant percentage of the daily Reference Nutrient Intake
recommendations for the consumption of dairy prod-                 of key nutrients to babies and children up to 10 years
ucts because of the strong evidence for the role of dairy          of age, providing, for example: 10%–19%             calcium,
products in meeting nutrient intake requirements.22 In             11%–20% phosphorus,             10%–21% riboflavin       and
both the USA and UK, current dietary guidelines recom-             17%–54% vitamin B12.27 Yogurts are often recommended
mend low-fat and low-sugar dairy products because of               to be part of children’s diets due to their high calcium
obesity-related concerns; however, a growing number of             content and its positive effect on bone development.28
recent studies suggest that high-fat dairy consumption is          Calcium also has a positive effect on teeth and high
associated with a lower risk of obesity and diabetes.21 23–25      intakes of milk and yogurt products in multiple studies
Large cohort studies in Sweden (n=1782 men 40–60 years             have been associated with reduced tooth erosion.29
old)23 and the USA (n=18 438 women ≥45 years old in                However, although there is good evidence to suggest that
the Women's Health Study)24 have found high-fat dairy              yogurt can be beneficial to health, products on the market
to be protective against developing central adiposity and          may vary widely in sugar content and yogurt marketed
becoming overweight or obese at follow-up. These data              specifically to children may be higher in free or added
have fed into ongoing wider debate regarding dietary               sugars (see table 1 for definitions of free, added and
guidance related to fat, refined carbohydrates and cardio-         total sugars).30 31 Dairy is a significant contributor to the
vascular disease risk.26                                           intakes of free sugars by children and adults.32 Diets high
                                                                                                                                               BMJ Open: first published as 10.1136/bmjopen-2017-021387 on 18 September 2018. Downloaded from http://bmjopen.bmj.com/ on 29 November 2018 by guest. Protected by copyright.
in free sugars are now unequivocally linked to obesity                      panna cotta, chilled soya desserts, quark, egg custards’,39
and dental caries, prompting the WHO and other regu-                        we chose to include these products in the analyses here.
latory bodies in updating dietary guidelines to strongly                    Therefore, the dessert category contains both yogurt-
advocate for restricting free sugar intakes to less than                    based and other products (eg, jellies and puddings, ie,
10% of total energy.33 34 With an alarming 58% of women                     chocolate mousse, crème caramels) that contain no
and 68% of men along with one in three of UK children                       yogurt or fromage frais cultures. However, non-yo-
aged 10–11 years overweight or obese in 2015,35 the UK’s                    gurt (eg, high-protein) drinks were removed from the
guidelines more stringently recommended the restric-                        nutrient analyses. Soya-based yogurts were placed in the
tion of free sugars to less than 5% of total daily energy.36                'dairy alternative’ category, whereas Greek-style yogurts
As part of a plan to combat childhood obesity, in April                     with added honey or other sweeteners were placed in
2018 the UK government implemented an industry soft                         the ‘flavoured’ category. ‘Fruit’ was defined liberally, for
drinks levy and commissioned a structured programme                         example, many products were made with either curd or
of monitored sugar reduction as part of wider refor-                        purees and for lemon products in particular, often with
mulation tackling calories, salt and saturated fat.37 The                   juice. In the case of natural yogurts, if organic, they went
initial focus was on the top nine food categories (after                    in organic category. In scrutinising the children’s cate-
soft drinks and fruit juices and smoothies) that contribute                 gory (products included were defined as ‘children’s’
the most to children’s sugar intakes. These are: chocolate,                 if either the supermarket or product itself defined it as
confectionery, biscuits, breakfast cereals, cakes, morning                  such, or if spokescharacters, celebrities, cartoons, toy
goods (such as croissants, buns and waffles), ice cream,                    giveaways, games or kids’ clubs were incorporated into
yogurt and sweet spreads/sauces. yogurt was one of the                      brand image), the ingredient lists were used to evaluate
products identified and highlighted for a 20% reduction                     presence or absence of yogurt or fromage frais cultures.
of sugar by 2020, with guidelines given for energy per                         For the classification of low fat and low sugar, the cut-offs
portion size of 120 kcal sales weighted average; 175 kcal                   defined by European Union (EU) regulations2 currently
maximum per portion and an allowance made for lactose                       used for voluntary, front-of-pack, traffic light coloured
(3.8 g/100 g).37                                                            labels in the UK40 were used. In this scheme, green desig-
   In this context then, the aims of this work were to                      nates low, amber designates medium and red designates
perform a comprehensive survey of yogurt products                           high levels of reference intakes. Low fat is defined as ≤3 g
within the major UK supermarkets, in order to identify                      of fat/100 g or ≤1.5 g/100 mL for drinks; low sugar is
products marketed at children and to evaluate their
nutrient contents, in particular sugar, compared with
other categories.
Experimental methods
Data collection
Data were collected from five major UK online super-
markets (Asda, Morrisons, Sainsbury’s, Tesco and Wait-
rose) that account for 75% of the UK grocery market
share.38 Websites were searched from 7 October 2016 to
16 November 2016 using ‘yogurt’ or ‘yoghurt’ as a search
term (in four of five supermarkets the same number of
products was returned). After considering the product
groupings commonly used by online supermarkets, eight
categories (children’s, dairy alternatives, dessert, drinks,
flavoured, fruit, natural/Greek, organic) and a systematic
process flow strategy for product placement (figure 1)
were decided on a priori. These product groupings, and
those typically used by supermarkets for both inventory
and marketing reasons, go beyond the standard broad
subgroupings used in dietary surveys such as the UK
National Dietary and Nutrition Survey (NDNS), where
the main food group ‘15: yogurt, fromage frais and other
dairy desserts’ has only three broad subsidiary groups of
either: ‘yogurt’; ‘manufactured fromage frais and other                     Figure 1  Process flow diagram of category decisions. Data
dairy desserts’; or ‘homemade fromage frais and other                       were collected using yogurt as a search term within the UK’s
dairy desserts’.39 As dairy desserts for the NDNS include                   top five online supermarkets between 7 October 2016 and
‘chocolate and fruit cream desserts, mousse, milk jelly,                    16 November 2016. Products were classified into different
junket, buttermilk desserts, fruit fools, crème caramel,                    categories as shown.
BMJ Open: first published as 10.1136/bmjopen-2017-021387 on 18 September 2018. Downloaded from http://bmjopen.bmj.com/ on 29 November 2018 by guest. Protected by copyright.
Figure 2  Nutrient and energy contents of UK yogurt products across categories. (A) Sugar. (B) Fat. (C) Protein. (D) Calcium.
(E) Energy. (F) Energy/serving. Data were tested for normality and analysed using the Kruskal-Wallis and Dunn’s multiple
comparison tests; categories with unlike letters were significantly different. Median is indicated by black line. Dashed lines
indicate thresholds defined by European Union (EU) regulations2 for nutrition claims for low sugar (A) and low fat (B).
defined by a maximum of 5 g total sugars/100 g. For label-         energy from sugars and is much higher than the recent
ling, high fat and high sugar (red) are defined at >17.5 g         UK and WHO targets of 5%–10% of energy from free
fat/100 g and >22.5 g sugar/100 g, respectively. Notably           sugars (25–50 g sugar/day in a 2000 kcal diet).2 40
for sugar, the current EU reference intakes are for 90 g             Data were screened for duplicates and a non-redun-
sugar in a 2000 kcal diet; this represents 18% of total            dant database of product information was created that
                                                                                                                                              BMJ Open: first published as 10.1136/bmjopen-2017-021387 on 18 September 2018. Downloaded from http://bmjopen.bmj.com/ on 29 November 2018 by guest. Protected by copyright.
 Table 2  Macronutrients across yogurt categories
                                        Fat                                 Carbohydrates (total sugars) Protein
                    n                   Median             Range            Median           Range         Median            Range
                                        (% energy)
 Children’s         101                 26.2*              19.9–40.8        52.0* (45.5)     25.4–57.9     20.0*             13.1–40.5
 Dairy
 alternatives         38                30.2*              21.9–86.3        50.8*† (48.4)    7.1–63.5      18.8*             2.4–40.0
 Dessert            161                 32.6*              0.0–63.1         55.0‡ (46.3)     29.0–100      10.8†             0.0–34.9
 Drinks               70                17.1†              0.0–54.8         62.4‡ (52.5)     25.6–95.2     15.8†             7.9–40.0
 Flavoured            79                31.7*              0.0–53.5         52.2*†  (45.8)   26.4–69.6     14.7†             0.0–70.0
 Fruit              317                 16.6†              0.0–53.5         56.8‡ (52.8)     25.5–78.1     17.7†             7.6–61.5
 Natural/Greek        61                25.9*              0.0–75.0         34.7† (30.4)     11.3–61.3     32.3‡             11.4–72.3
 Organic              71                33.4*              0.0–69.8         48.5*† (46.7)    16.4–73.5     17.5*             0.3–56.3
                                        (g/100  g)
 Children’s         101                 2.8*               1.9–5.7          12.3* (10.8)     4.9–25.0      5.3*              2.8–8.6
 Dairy
 alternatives         38                2.5*†              1.9–21.0         9.5* (9.2)       1.0–16.2      3.6†              0.6–5.2
 Dessert            161                 5.2†               0.0–26.7         19.6† (16.4)     6.3–54.9      4.0†‡             2.0–9.5
 Drinks               70                1.5‡               0.0–3.0          11.2* (9.1)      2.3–18.4      2.7†              1.3–5.9
 Flavoured            79                3.6*†              0.0–9.6          13.0* (12.0)     3.7–19.0      4.2*‡§            0.4–9.8
 Fruit              317                 1.6§               0.0–8.9          12.9* (11.9)     4.8–22.4      4.2§              2.1–10.0
 Natural/Greek        61                1.7*†§             0.0–10.2         5.5‡ (5.0)       3.6–9.5       5.4*              2.2–11.0
 Organic              71                3.9*†              0.0–10.1         13.3* (13.1)     4.8–22.7      4.5*§             3.0–7.6
 *†‡§Median values within a column with unlike superscript symbols were significantly different (p<0.0001) by Kruskal-Wallis and Dunn's
 multiple comparison tests.
included: nutrient information, serving size, size of pack,                  Patient and public involvement
claims on pack and ingredients. Nutrient information was                     Patients and the public were not involved in this research.
confirmed from the brand’s own website where possible
and a subset was examined during in-store visits. Informa-
tion on macronutrients, including energy, fat, saturated                     Results
fat, carbohydrates, sugar, fibre and protein, was collected,                 Nine hundred and twenty-one products identified online
as well as any information on micronutrients. Data for                       during the period of the survey were initially included
macronutrients have been expressed as g/100 g product                        in the analysis. At the time of survey, although national
as well as % energy, as both are needed to evaluate its                      branded products dominated the products available
nutritional merits; for example, a yogurt with a lower                       (n=648 national vs n=273 own brand products), only 65
energy content per 100 g may have a higher % energy                          products were available in all five supermarkets. Following
from sugar than a product with a higher energy content.                      the process flow strategy (figure 1) removed 23 non-yo-
All data were independently double-checked and 5% of                         gurt, for example, high protein type, beverages from the
all entries were randomly selected and verified.                             analyses and the remaining 898 products were classed
                                                                             as either: children’s (n=101), dairy alternatives (n=38),
Data analysis                                                                dessert (n=161), drinks (n=70), flavoured (n=79), fruit
Pivot tables in Excel were used for building and manip-                      (n=317), natural/Greek (n=61) or organic (n=71).
ulating the product database and statistical analyses                          In assessing nutrient contents across the surveyed prod-
were done utilising GraphPad Prism V.7.0 c. Normality                        ucts, the sugar content varied enormously both within
was examined using the D’Agostino-Pearson omnibus                            and across our product categories (figure 2A). With the
normality test and comparisons across all categories were                    exception of the natural/Greek category, the median
made using the non-parametric Kruskal-Wallis test with                       total sugar contents of all categories were well above the
Dunn’s multiple comparisons. For comparisons of two                          5 g/100 g maximal threshold considered for a low-sugar
categories, again in not observing normal distributions,                     nutrition label claim.2 40 Products within the dessert
the non-parametric, two-tailed Mann-Whitney tests were                       category, unsurprisingly, had the highest median and
applied.                                                                     broadest (range) of total sugar at 16.4 g/100 g (1.5–32.6)
                                                                                                                                                BMJ Open: first published as 10.1136/bmjopen-2017-021387 on 18 September 2018. Downloaded from http://bmjopen.bmj.com/ on 29 November 2018 by guest. Protected by copyright.
                                                                   threshold with medians for fat of 3.6 g/100 g (0, 9.6) and
                                                                   3.9 g/100 g (0, 10.1), respectively, the dessert category
                                                                   contained the highest median amount of fat and had the
                                                                   broadest range at 5.2 g/100 g (0–26.7) (figure 2B). The
                                                                   drinks category had the lowest median fat contents at
                                                                   1.5 g/100 g (0, 3.0), but the fruit and natural/Greek cate-
                                                                   gories were also relatively low with medians of 1.6 (0, 8.9)
                                                                   and 1.7 (0, 10.1) g/100 g, respectively (figure 2B).
                                                                     The natural/Greek and the children’s categories
                                                                   had the highest median protein contents at 5.4 (2.2,
                                                                   11.0) and 5.3 (2.8, 8.6) g/100 g yogurt (figure 2C).
                                                                   The higher protein median for the children’s category
                                                                   was influenced, as expanded on below, to a significant
                                                                   degree by a large percentage of higher protein fromage
                                                                   frais products. The dessert, fruit, flavoured and organic
                                                                   categories had very similar median protein contents
                                                                   at 4.0–4.5 g/100 g, whereas drinks and dairy alternatives
                                                                   contained the least amount of protein at 2.7 (1.3, 5.9)
                                                                   and 3.6 (0.6, 5.2) g/100 g (figure 2C). Calcium values
                                                                   were less frequently reported, but median values between
                                                                   yogurt categories were broadly similar ranging from 116
                                                                   to 150 mg/100 g (figure 2D). Mimicking protein, the
                                                                   natural/Greek and the children’s categories had the
                                                                   highest calcium contents. The dessert category, again not
                                                                   surprisingly, contained significantly more energy/100 g
                                                                   (figure 2E) and more energy/serving (figure 2F) than any
                                                                   other category. Although the children’s category had the
                                                                   least energy/serving (figure 2F), this was clearly due to
                                                                   smaller serving sizes. When expressed as kcal/100 g, the
Figure 3  Macronutrients compared across low-fat                   median energy of children’s yogurts was similar to prod-
(≤3 g/100 g; n=530) and higher fat (>3 g/100 g; n=383)             ucts in the dairy alternative, flavoured, fruit and organic
products. (A) Sugar. (B) Fat. (C) Protein. (D) Energy. Data were   categories (ranging from 79 to 100 g/100 g), and these
tested for normality and analysed using the Mann-Whitney
                                                                   were significantly higher than the median (65 g/100 g) of
test. Median is indicated by black line. ****P<0.0001.
                                                                   the natural/Greek category (figure 2E).
                                                                     In examining the macronutrient content (as % energy)
(figure 2A). However, the children’s, flavoured, fruit and         of yogurts across categories, it was clear that the majority
organic categories all had relatively high, and similar,           of carbohydrates in yogurt products are derived from
median total sugar contents ranging from 10.8 g/100 g              sugars (table 2). Carbohydrate content ranged from the
(children’s) to 13.1 g/100 g (organic). As the natural/            extremes of 34.7% (natural/Greek) to 62.4% (drinks)
Greek category by definition contained no added sweet-             of energy content, but all other categories were tightly
eners, it had the lowest median amount of total sugars             bunched at 48.5%–56.7%        carbohydrate content. The
per product (5 g/100 g (1.6, 9.5)). These sugars will              natural/Greek category was significantly higher in
be ~80% lactose (table 1), but notably the range observed          protein (32.3%) than any other category, while the dessert
here suggests many products will have higher than the              category had the least amount of protein (10.8%) and
allowance of 3.8 g/100 g specified for lactose in the UK           highest percentage of fat (32.6%; table 2). Although fruit
sugar reduction programme guidelines. The dairy alter-             and flavoured yogurts had very similar sugar contents
natives and drinks categories also had total sugar medians         (table 2), fruit yogurts contained small, but appreciably
higher than 5 g/100 g, nonetheless these were still signifi-       more, amounts of fibre compared with flavoured or
cantly lower than the children’s, flavoured, fruit and             natural/Greek yogurts (0.3 (0, 2.4) vs 0 (0, 0.9) g/100 g).
organic categories with median (range) of 9.2 g/100 g                It has previously been reported from an analysis of a US
(0.4–12.5) for dairy alternatives and 9.1 g/100 g (2.3–            database that low-fat products, including yogurts, contain
16.5) for drinks (figure 2A).                                      more sugar than their higher fat counterparts.41 However,
   Somewhat in contrast to sugar, as seen in figure 2B, many       in comparing products below (n=518) and above (n=380)
yogurt categories (children’s, dairy alternative, drinks,          the  ≤3 g/100 g threshold for low-fat product labelling,
fruit, natural/Greek) had median levels of fat lower               we did not observe this here. Low-fat yogurt products
than the thresholds considered ‘low-fat’ for nutrition             had significantly lower amounts of sugar in comparison
claims (3 g/100 g for food and 1.5 g/100 mL for drinks).2          to higher fat yogurts (10.7 (0.1, 21.5) vs 13.1 (0, 32.6)
While flavoured and organic yogurts were just over this            g/100 g; figure 3A) and much lower median and tighter
                                                                                                                                           BMJ Open: first published as 10.1136/bmjopen-2017-021387 on 18 September 2018. Downloaded from http://bmjopen.bmj.com/ on 29 November 2018 by guest. Protected by copyright.
Figure 4  Nutrients in children’s yogurt (n=39) and fromage frais (F Frais; n=62) products. (A) Sugar. (B) Fat. (C) Protein. (D)
Calcium. (E) Energy. (F) Energy/serving. Data were tested for normality and analysed using the Mann-Whitney test. Median is
indicated by black line. **P<0.01; ***P<0.001; ****P<0.0001.
range of fat contents (1.4 (0–3.0) vs 5.5 (1.6–26.7)                        products marketed to children. Our results highlight that
g/100 g; figure 3B). Low-fat yogurts contained more                         the total sugar content of yogurts is relatively high in all
protein than higher fat products (4.3 (0, 11.0) vs 3.9 (0.1,                categories, with the exception of natural/Greek yogurts.
9.5) g/100 g; figure 3C) and much lower energy per 100 g                    Very few products, less than 9%, qualified for a low-sugar
(81 (28, 143) vs 125 (36, 445) g/100 g; figure 3D).                         (≤5 g/100 g) claim for front-of-pack labelling, and almost
   While fromage frais is also a fresh lactic fermented                     none in the children’s category. This is concerning given
milk product, it is made with cheese cultures rather                        both the continued increase in childhood obesity and
than yogurt cultures. In most of the categories, less than                  prevalence of tooth decay among children starting school
5% of products were fromage frais and were not sepa-                        (28%).42 Tooth extractions are shockingly the primary
rated out. However, in the children’s category, fromage                     reason children aged 5–9 are admitted to hospital with
frais dominated, representing 60% of products (n=62 vs                      general anaesthetic in the UK.43 Moreover, in 2015/2016
n=39 yogurts) so their nutrient contents were assessed                      more than one in five children in Reception (ages 4–6),
separately (figure 4). While there was no difference                        and one in three children in Year 6 (ages 10–12) were
in the sugar content of children’s yogurt and fromage                       measured as obese or overweight in England.44 While
frais (figure 4A), fromage frais products had lower
                                                                            yogurt may be less of a concern than soft drinks and fruit
fat (figure 4B; p<0.0001), higher protein (figure 4C;
                                                                            juices, the chief sources of free sugars in both children
p<0.0001) and higher calcium (figure 4D; p<0.01)
                                                                            and adult’s diets,39 what is worrisome is that yogurt, as a
contents compared with children’s yogurts. Although
                                                                            perceived ‘healthy food’, may be an unrecognised source
there was no difference in energy/100 g (figure 4E), the
                                                                            of free/added sugars in the diet. Indeed, a potentially
energy/serving was significantly lower for fromage frais
(figure 4F; p<0.0001) reflecting its often smaller serving                  surprising observation from our data was that, after the
size.                                                                       dessert category, it was organic yogurts that had the
                                                                            highest median sugar content (13.1 g/100 g). While the
                                                                            organic label refers to production, the well-documented
Discussion                                                                  ‘health halo’ effect means that consumers most often
We have comprehensively evaluated yogurt products sold                      underestimate the caloric content and perceive the nutri-
in the major UK supermarkets in November 2016, exam-                        tional contents of organic products, including yogurts,
ining nutrient contents across categories, including those                  more favourably.45
                                                                                                                                              BMJ Open: first published as 10.1136/bmjopen-2017-021387 on 18 September 2018. Downloaded from http://bmjopen.bmj.com/ on 29 November 2018 by guest. Protected by copyright.
   An additional challenge for even an educated consumer         20% reduction aim for 11.0 g/100 g product; the report
is understanding that the total sugars on the label include,     suggests reformulation, reducing portion size and shifting
in the case of yogurt, the intrinsic milk sugar, lactose, plus   portfolio of sales are all viable mechanisms to help achieve
sugars added as sweeteners during processing. UK label-          this.37 While median sugar values are not directly compa-
ling laws do not require the declaration of free sugars          rable to sales weighted averages, our study suggests the
on nutrition labels and the UK’s sugar reduction guide-          organic (13.1 g/100 g), fruit (11.9 g/100 g) and flavoured
lines focus on total sugars for this reason. Interestingly,      (12.0 g/100 g) categories require the greatest changes.
although some have argued it is difficult to measure, the        Children’s yogurt and fromage frais products had a some-
inclusion of added sugars (under total sugars) on food           what lower median of sugar 10.8 g/100 g, possibly meeting
labels has been recently mandated in the USA; companies          government guidelines (not clear as not sales weighted).
have until 2020 or 2021 to implement depending on their          However, given the recommendations that 4–6 year-olds
size.46 Notably, added sugars in the USA do not include          should have no more than 19 g of sugar a day, a single
the sugars in juiced or pureed fruits and vegetables that        pot of yogurt can contribute substantially to sugar intakes
are defined as free sugars by the UK and WHO. It has             of children. The sugar content of children’s yogurts
been argued for public health purposes, the emphasis             and fromage frais varied dramatically and there was no
in communication should be free sugars,47 and it will            difference between the sugar contents of yogurts and
be interesting to see how food product companies and             fromage frais per 100 g of product. However, as fromage
consumers navigate these changes. Our study highlighted          frais has a much smaller serving size (median 47 g vs 90 g
other potential challenges and mixed messages for                for yogurt), fromage frais products contained much less
consumers, arising from marketing and packaging. Many            sugar per serving than yogurt (5.4 vs 9.2 g sugar/serving);
products that were suggested for children’s lunch boxes          with a single serving of yogurt on average delivering close
on supermarket websites were very high-sugar desserts            to half of a child’s daily maximal recommended intake of
(from jelly to dairy based) rather than yogurt or fromage        sugar.
frais. Retailers could play a positive role in promoting           Reformulation is likely to be challenging; beyond acting
health here by establishing boundaries for inclusion in          as a sweetener, added sugar in foods acts as a bulking and
lunch box recommendations. Furthermore, the portion              colouring agent, and the use of sugar in foods is dictated
sizes for children’s yogurts varied enormously and were          by physical and chemical properties that are difficult to
often identical to adult portion sizes. Equally there was        substitute.49 In addition, in general consumers ‘liking’
little consistency in portion size in adult yogurts either,      for yogurt is correlated positively with sweetness.50 Lactic
and particularly for larger pots (400–500 g) of yogurt the       fermentation yields a sour taste that sugar attenuates.
serving size was either not given or was different from the      Consumers have been shown to prefer yogurt containing
equivalent smaller pot of yogurts (100–150 g/serving).           10%–13% added sugar but may accept products with
In multiple products with added plant stanols marketed           7% added sugar while rejecting products with 5% or less
for their cholesterol-lowering merits, none would meet           added sugars as too sour, or adding sweeteners (caster
a low-sugar claim and several were extremely high in             sugar, jam or honey) themselves before consuming.50–53
sugar. In light of data linking high sugar consumption to        When Saint-Eve and colleagues53 precisely measured
high cholesterol levels,48 arguably these products should        sugar added by 204 French subjects to natural yogurt they
be scrutinised for reformulation with a view to poten-           found on average participants added 13.6 g of sugar to
tial added health benefits in terms of obesity and dental        their yogurts, more than total content of many commer-
caries.                                                          cial sweetened yogurts. Participants underestimated how
   The UK guidelines for sugar reduction in the yogurt           much sugar they were adding but still perceived their
and fromage frais category do not apply to dairy desserts,       addition of sweetener to be the healthier option.53
natural/unsweetened yogurt/fromage frais and yogurt/               Although we have focused our attention on the sugar
dairy drinks (although ‘any sugar-sweetened yogurt               content of yogurts per se, it is important to consider
and dairy drinks that are excluded from the soft drinks          other nutrients, not least because of the impact on the
industry levy will become part of the sugar reduc-               glycaemic response. Notably, our work illustrates that
tion programme’).37 But it was interesting to note the           natural/Greek yogurts have a dramatically different
median of sugar content in plain, natural/Greek yogurts          macronutrient profile from all other categories,
(5.0 g/100 g), which is predominantly lactose, was higher        containing much higher protein (32.4% energy vs range
than the allowance of 3.8 g/100 g that the UK guidelines         of 10.8%–20%) and much lower carbohydrate (34.7% vs
agreed on for lactose. It should be noted that the guide-        48.5%–60.4%) than all other categories. The observed
lines have been made, in consultation with industry, on          glycaemic index (GI) of yogurts is generally much lower
sales weighted averages so are not directly comparable           than predicted values calculated from their carbohydrate
here. This is calculated by weighting the sugar level of         contents, with unsweetened yogurts having the lowest
individual products by their volume sales, so that high-         GI of all; this is contributed both to the fact that lactose
selling products with high sugar levels will push sales          has a low GI, and because yogurts’ protein content will
weighted average upwards. For yogurt, the reported               reduce the glycaemic response.54 Similarly, while some
baseline sales weighted average was 12.8 g/100 g, with a         studies suggest lactose may be less cariogenic than other
                                                                                                                                                                   BMJ Open: first published as 10.1136/bmjopen-2017-021387 on 18 September 2018. Downloaded from http://bmjopen.bmj.com/ on 29 November 2018 by guest. Protected by copyright.
sugars,55 it is recognised that the food components in                      narrow a time frame as possible and we took only a month
unsweetened dairy products provide a buffering capacity                     here. However, manufacturers may have made changes to
that is protective to teeth enamel.56 We might underscore,                  products since this snapshot and it would be interesting
therefore, that it is yogurts sweetened with added sugars                   to repeat the survey in future years. As nutrient data were
that are primarily of concern here. In particular perhaps,                  collected from online information, provided by super-
for young children who derive a significant amount of                       markets or the brand’s own website, these data may not
their free sugar intake, which does not include lactose,                    always be up to date or accurate. We did not incorporate
from yogurt products (12% for 1.5–4 year-olds and 6%                        analysis of price here; it would be interesting to assess if
for 4–10 year-olds),39 at a time when taste preferences are                 sugar or other nutrients relate to price.
being established for life.57 Yogurt without added sugars
remains a nutritious food for all ages and should ideally
be introduced unsweetened during early childhood                            Conclusions
weaning. Although a drop in daily free sugars intake in                     While there is good evidence that yogurt can be bene-
the UK has been recently observed, currently consump-                       ficial to health, products on the market vary widely in
tion is well over 10% in all age groups, much higher than                   nutrient content. In a comprehensive survey of the UK
the 5% target.39 While clearly in terms of dietary sugar                    supermarket yogurt products, we highlight here that
intakes and obesity or dental caries, yogurt is not the                     the median sugar contents of children’s, fruit, flavoured
concern sugar sweetened beverages are, which contribute                     and organic yogurt categories were well above 10 g/100 g
to 25%–40% of free sugar intake in 1.5–4 year-olds,39                       and represented >45% of total energy derived. Organic
nonetheless the rationale for reduction and reformula-                      yogurts (including organic yogurt with added fruit or
tion across a broad range of products as part of a systemic                 flavourings, and so on) had the highest median sugar
approach to prevent obesity is robust.34 58                                 content (13.1 g/100 g). Notably, natural/Greek yogurts
   We had preconceived that low-fat yogurts would                           had a dramatically different macronutrient profile from
contain more sugar than their higher fat alternatives,                      all other categories, containing much higher protein
in part because of a previous, short report from an                         (32.4% vs range of 10.8%–20% energy) and much lower
American database analysis that showed low-fat prod-                        carbohydrate (34.7% vs 48.5%–60.4% energy) contents
ucts, including yogurts, contain more sugar than their                      than all other categories. While natural/Greek yogurts
higher fat counterparts.41 In contrast, low-fat prod-                       contained the least amount of sugars, their median
ucts surveyed here had significantly lower sugar than                       total sugar (5.0   g/100 g, largely lactose) was higher
higher fat products (10.3 vs 13.1 g/100 g in higher fat).                   than the agreed allowance (3.8      g/100 g) for lactose.
However, we note that although low-fat products did have                    Although low-fat products had less sugar and energy than
less sugar on average, nonetheless 55% of low-fat prod-                     higher fat yogurts, nonetheless 55% of low-fat products
ucts had between 10 and 20 g sugar/100 g. With an energy                    contained 10–20 g sugar/100 g. Within the children’s
intake of 2000 kcal/day, 5% of energy amounts to 25 g                       category, fromage frais had higher protein and calcium
of sugar, and a single serving of yogurt in all categories                  contents/100   g than yogurts and was marketed with
surveyed, other than natural/Greek, can easily provide                      smaller serving sizes. Less than 9%, and only 2% of chil-
half or more of this. On the other hand, a 150 g serving                    dren’s, products surveyed were low enough in sugar to
of the median sugar (16.4 g/100 g) dessert product could                    earn ‘green’ in UK front-of-the pack labelling; and many
provide a person the recommended 25 g daily limit of                        products recommended by supermarkets for lunch boxes
sugar. Nonetheless, low-fat products had lower energy, fat                  were high-sugar desserts. We conclude not all yogurts are
and sugar contents, and were slightly higher in protein, in                 as healthy as perhaps consumers perceive them and refor-
comparison to higher fat products. This profile appears                     mulation for the reduction of free sugars is warranted.
consistent with current UK and US dietary guidelines
that recommend low-fat dairy products out of concerns                       Contributors  JBM designed the study, analysed the data and wrote the
for obesity and cardiovascular disease. It is notable that                  manuscript. AH carried out the study, analysed the data and contributed to a
                                                                            preliminary draft. BAF helped design and interpret the study and revised the
evidence is accumulating that higher fat, rather than                       manuscript critically for important intellectual content.
low-fat, dairy is associated with a lower risk of obesity and
                                                                            Funding  This research received no specific grant from any funding agency in the
diabetes,21 23–25 including several studies that suggest full               public, commercial or not-for-profit sectors.
fat milk is associated with reduced risk of overweight and
                                                                            Competing interests  None declared.
obesity in children.25 59 60
                                                                            Patient consent  Not required.
   The study has some limitations. We would have liked to
have included products sold outside the five major online                   Provenance and peer review  Not commissioned; externally peer reviewed.
supermarkets but this would have created difficulties in                    Data sharing statement  No additional data are available.
data collections and setting the boundary of inclusion.                     Open access This is an open access article distributed in accordance with the
However, the supermarkets included covered 75% of the                       Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which
                                                                            permits others to distribute, remix, adapt, build upon this work non-commercially,
grocery market and is therefore representative of the                       and license their derivative works on different terms, provided the original work is
overall market, and as such provides a useful database for                  properly cited, appropriate credit is given, any changes made indicated, and the use
discussion. Ideally data collection should take place in as                 is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/.
                                                                                                                                                                             BMJ Open: first published as 10.1136/bmjopen-2017-021387 on 18 September 2018. Downloaded from http://bmjopen.bmj.com/ on 29 November 2018 by guest. Protected by copyright.
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