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835
Appl. Physiol. Nutr. Metab. Downloaded from www.nrcresearchpress.com by Periodicals Publicacoes Tecnicas on 10/20/16
For personal use only.
ARTICLE
Associations between added sugar (solid vs. liquid) intakes,
diet quality, and adiposity indicators in Canadian children
JiaWei Wang, Lei Shang, Kelly Light, Jennifer O’Loughlin, Gilles Paradis, and Katherine Gray-Donald
Abstract: Little is known about the influence of different forms of added sugar intake on diet quality or their association with
obesity among youth. Dietary intake was assessed by three 24-h recalls in 613 Canadian children (aged 8–10 years). Added sugars
(mean of 3-day intakes) were categorized according to source (solid or liquid). Dietary intake and the Canadian Healthy Eating
Index (« HEI-C ») were compared across tertiles of solid and liquid added sugars separately as were adiposity indicators (body mass
index (BMI), fat mass (dual-energy X-ray absorptiometry), and waist circumference). Cross-sectional associations were examined in
linear regression models adjusting for age, sex, energy intake, and physical activity (7-day accelerometer). Added sugar contributed 12% of total energy intake (204 kcal) on average, of which 78% was from solid sources. Higher consumption of added sugars
from either solid or liquid source was associated with higher total energy, lower intake of micronutrients, vegetables and fruit,
and lower HEI-C score. Additionally liquid sources were associated with lower intake of dairy products. A 10-g higher consumption of added sugars from liquid sources was associated with 0.4 serving/day lower of vegetables and fruit, 0.4-kg/m2 higher BMI,
a 0.5-kg higher fat mass, and a 0.9-cm higher waist circumference whereas the associations of added sugars from solid sources
and adiposity indicators tended to be negative. In conclusion, higher consumption of added sugar from either solid or liquid
sources was associated with lower overall diet quality. Adiposity indicators were only positively associated with added sugars
from liquid sources.
Key words: added sugars, diet quality, obesity, children, Healthy Eating Index.
Résumé : Il y a peu d’études au sujet de l’influence de l’ajout de sucre sous diverses formes sur la qualité du régime alimentaire
et de sa relation avec l’obésité chez les jeunes. On évalue l’apport alimentaire au moyen de trois carnets de rappel de 24 h chez
613 enfants canadiens (âgé de 8–10 ans). On classifie l’ajout de sucres (moyenne de l’apport durant 3 jours) en fonction de la
source : liquide ou solide. On compare l’apport alimentaire et l’Indice de saine alimentation au Canada (« HEI-C ») en fonction des
tertiles de sucres ajoutés sous forme liquide ou solide et on compare aussi les indicateurs de l’obésité (indice de masse corporelle
(IMC), masse adipeuse, absorptiométrie à rayons X en double énergie) et le tour de taille. On examine les relations transversales
au moyen de modèles de régression linéaire ajustés selon l’âge, le sexe, l’apport alimentaire et l’activité physique (accélérométrie
durant 7 jours). Le sucre ajouté compte en moyenne pour 12 % de l’apport énergétique total (204 kcal) et 78 % provient d’aliments
solides. Une consommation plus élevée de sucres ajoutés provenant de sources liquides ou solides est associée à un plus grand
apport énergétique total, à un plus faible apport de micronutriments, de fruits et légumes et à un résultat plus faible à l’HEI-C.
De plus, les sources liquides de sucres sont associées à un plus faible apport en produits laitiers. Une consommation supplémentaire de 10 g de sucres de sources liquides est associée à une diminution de 0,4 portion par jour de fruits et légumes, à un IMC
supérieur de 0,4 kg/m2, à 0,5 g de plus de masse adipeuse et à 0,9 cm de plus de tour de taille; par contre, les associations entre
les sucres ajoutés de sources solides et les indicateurs de l’adiposité présentent une tendance négative. En conclusion, une plus
forte consommation de sucres ajoutés de sources liquides ou solides est associée à une plus faible qualité globale de
l’alimentation. Les indicateurs de l’adiposité sont les seules variables positivement associées aux sucres ajoutés de sources
liquides. [Traduit par la Rédaction]
Mots-clés : sucres ajoutés, qualité de l’alimentation, obésité, enfants, indice de saine alimentation.
Introduction
A healthy diet is essential for normal growth in children and
adolescents, and helps prevent obesity and related chronic diseases (Committee on Food Marketing and the Diets of Children
and Youth 2006). Although Canadian youth consume adequate
amounts of most nutrients, insufficient intake of some essential
micronutrients is still evident. For example, the prevalence of
inadequate vitamin A, magnesium, zinc, and phosphorus ranges
between 10%–30%, and even as high as 67% for calcium among
Canadian youth aged 9 to 13 years (Health Canada 2012). Childhood obesity has become a major public health concern around
Received 21 October 2014. Accepted 15 March 2015.
J.W. Wang* and K. Light. School of Dietetics and Human Nutrition, McGill University, Ste-Anne-de-Bellevue, QC H9X 3V9, Canada.
L. Shang. School of Dietetics and Human Nutrition, McGill University, Ste-Anne-de-Bellevue, QC H9X 3V9, Canada; Department of Health Statistics,
Faculty of Preventive Medicine, Fourth Military Medical University, Xi’an, 710032 China.
J. O’Loughlin. Department of Social and Preventive Medicine, University of Montreal, Montreal, QC H3C 3J7, Canada; University of Montreal Hospital
Research Centre (CRCHUM), Montreal, QC H2X 0A9, Canada.
G. Paradis. Department of Epidemiology, Biostatistics and Occupational Health, McGill University, Montreal, QC H3A 1A2, Canada.
K. Gray-Donald. School of Dietetics and Human Nutrition, McGill University, Ste-Anne-de-Bellevue, QC H9X 3V9, Canada; Department of
Epidemiology, Biostatistics and Occupational Health, McGill University, Montreal, QC H3A 1A2, Canada.
Corresponding author: Katherine Gray-Donald (e-mail: [email protected]).
*Present address: Department of Applied Human Nutrition, Mount Saint Vincent University, Halifax, NS B3M 2J6, Canada.
Appl. Physiol. Nutr. Metab. 40: 835–841 (2015) dx.doi.org/10.1139/apnm-2014-0447
Published at www.nrcresearchpress.com/apnm on 14 April 2015.
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836
the world. In Canada, 8.0% of children aged 6 to 11 years and 9.4%
of adolescents aged 12–17 years are classified as obese (age- and
sex-specific body mass index (BMI) ≥95th percentile) (Roberts et al.
2012). In recent decades, diets across the world are sweetening,
with dramatic increases in the consumption of added sugars
(Popkin and Nielsen 2003). American children aged 9 to 13 years
consumed as high as 419 kcal of added sugar per day (National
Cancer Institute 2014). Based on the data from 2004 Canadian
Community Health Survey, boys aged 9 to 13 years consumed
620 kcal of total sugars per day (which contributed 25.3% of their
daily calories), while teenage boys aged 14 to 18 years consumed the
highest amount of total sugars among all age groups (688 kcal/day),
with regular soft drinks as their primary source (Langlois and
Garriguet 2011).
Although recent United States data show declines in the consumption of added sugars, the average intake remains high in
youth (Welsh et al. 2011). Added sugars are defined as caloric
sweeteners added in the processing or preparation of foods and
beverages (Johnson et al. 2009). More than 60% of daily added
sugar intake comes from solid food (Langlois and Garriguet 2011),
and the top sources include grain-based desserts, dairy desserts,
candies, and ready-to-eat cereals (National Cancer Institute 2014).
Sugar-sweetened beverages (SSB) are the main liquid source of
added sugars in youths’ diet in North America (Guthrie and
Morton 2000; Garriguet 2008a). Flavoured milk is the other liquid
source of added sugars that is particularly prevalent among
school-aged youth. Among New York City public schools in 2009,
chocolate milk accounted for approximately 60% of total milk
purchased (Centers for Disease Control and Prevention (CDC)
2010).
There is evidence in some (Øverby et al. 2004; Joyce and Gibney
2008) but not all (Gibson 1993; Forshee and Storey 2001; Johnson
et al. 2007; Rennie and Livingstone 2007) studies that higher intake of added sugars reduces micronutrient intake, displaces
nutrient-dense foods, and is associated with obesity and weight
gain in youth. Forshee et al., using data from the Continuing
Survey of Food Intake by Individuals (1994–1996), reported that
the role of added sugars in the diet quality of children and adolescents is inconsistent and small (Forshee and Storey 2001). In addition, a longitudinal study of 1203 British children reported no
association between SSB consumption at age 5 or 7 years and total
fat mass at 9 years (Johnson et al. 2007). Previous studies relating
added sugars to dietary intake and health outcomes generally
study added sugars overall or only from liquid food sources (i.e.,
SSB and/or flavoured milk) (Johnson et al. 2009; Kynde et al. 2010).
Because most added sugars are from solid food sources, the importance of examining their role as well as SSB is recognized in a
recent statement by the American Heart Association (Johnson
et al. 2009). The present study was undertaken in a sample of
Canadian children at risk of obesity in that at least one of their
biological parents was obese. We studied the association of added
sugar intake from solid and liquid food sources on overall diet
quality and the associations between these 2 forms of added sugars and adiposity indicators.
Materials and methods
Study population
This study is a secondary data analysis of 630 children aged 8 to
10 years at baseline (2005–2008) participating in the QUebec Adipose and Lifestyle InvesTigation in Youth (QUALITY) study. Methods for this study have been described in detail elsewhere
(Lambert et al. 2012; Wang et al. 2013, 2014). Data were collected
during a clinic visit followed by telephone contacts. The study was
conducted according to the guidelines laid down in the TriCouncil Statement on Ethical Conduct of Research and all procedures involving human subjects were approved by the ethics
review boards at Centre Hospitalier Universitaire Sainte-Justine
Appl. Physiol. Nutr. Metab. Vol. 40, 2015
and Laval University. Written informed consent was obtained
from parents and assent was obtained from the children.
Dietary assessment
Within 8–12 weeks after the clinic visit, children’s dietary assessment on 2 weekdays and 1 weekend day was performed by a
registered dietitian through telephone interview. In all, 613 out of
630 children completed three 24-h dietary recalls. In this study,
the United States Department of Agriculture (USDA) Database for
the Added Sugars Content of Selected Foods (USDA 2006) was used
as the main data source for added sugars. Values of added sugars
for each food item were entered into CANDAT nutrient analysis
software version 8.0 (Godin London Inc., London, Ont., Canada).
All further dietary analyses, including food group creation and
nutrient calculation, were undertaken using CANDAT, which
bases food composition data on the Canadian Nutrition File version 2007b and 2010 (Health Canada 2010).
All food items were categorized by sources of added sugar into
24 food groups. Solid sources included added sugar from the following food groups: dairy and egg products; spices and herbs; fats
and oils; poultry products; soups, sauces, and gravies; sausages
and luncheon meats; ready-to-eat cereals; fruits; pork products;
vegetables and vegetable products; nuts and seeds; beef products;
fish and shellfish products; legumes and legume products; lamb,
veal, and game; baked products; sweets; cereals, grains and pasta;
fast foods; mixed dishes; and other snack foods. Liquid sources
included SSB and flavoured milk (Wang et al. 2014).
The Healthy Eating Index (HEI) is a measure of overall diet
quality that assesses conformance to the Dietary Guidelines for
Americans (Guenther et al. 2013). In Canada, a similar index of
HEI-C 2009 (Woodruff and Hanning 2010) was adapted based on
the latest dietary recommendation, Eating Well with Canada’s Food
Guide (Katamay et al. 2007). This HEI-C 2009 directly listed the
scoring scheme for 9- to 13-year-old youth, which includes 9 components with a continuous score assigned to each component, for
a maximum score of 100. One of its components, “other foods”
(10% of total score), mainly comprises foods rich in added sugars or
solid fats, which contribute excess calories and may displace
nutrient-dense foods from the diet. An overall higher score indicates closer conformity with Canada’s Food Guide, and a “good
diet” is defined as HEI-C score ≥80 points (Glanville and McIntyre
2006).
Adiposity assessment
Height, measured using a stadiometer with participants standing against a wall and looking straight ahead, was recorded to the
nearest millimetre during maximal inspiration. Weight was measured to the nearest 0.1 kg using an electronic scale, with participants wearing light indoor clothing and no shoes. BMI was
calculated as weight (kg)/height (m2) and age- and sex-specific BMI
z scores were determined using the growth charts published
by the United States CDC (Ogden et al. 2002). Dual-energy X-ray
absorptiometry (DXA) (Prodigy Bone Densitometer System,
DF+14664, GE Lunar Corp., USA) was used to assess fat mass. Waist
circumference was measured using a standard tape at the middistance between the last floating rib and the iliac crest at the end
of a normal expiration.
Physical activity assessment
To obtain objective measures of physical activity, children wore
a uniaxial activity monitor (Actigraph LLC, Pensacola, Fla., USA)
for a 7-day period following the clinic visit. The accelerometer was
worn for a mean of 13.4 h daily and recorded as counts per minute
(Corder et al. 2007). Being consistent with current procedures
used by the Canadian Health Measures Survey (Colley et al. 2011),
days were excluded when the accelerometer was worn for less
than 10 h and data from subjects who had worn the accelerometers for less than 4 days were excluded. Ninety-seven percent of
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Wang et al.
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children had more than 4 days of accelerometer data, which has
been shown to ensure adequate reliability (Puyau et al. 2002).
Actigraph accelerometers have been validated against activitybased energy expenditure assessed by doubly labelled water in
9-year-old children (r = 0.58) (Ekelund et al. 2001).
Statistical analysis
The calculated mean intake values from 3 recalls were used in
the analyses. The distribution of added sugars from solid and
liquid food sources was described as the percentage of total added
sugars. Participants were categorized according to tertile based on
the grams of added sugars consumed from solid or liquid food
sources. Daily average intake of nutrients (total energy, percentage of energy from protein, fat and carbohydrate, calcium, vitamins A and D), 2 food groups (milk and dairy products, vegetables
and fruit) and total HEI-C scores were compared across tertile of
added sugars from solid and liquid food sources separately using
ANOVA. ␹2 tests were used to compare the percentage of consuming a good diet across added sugar tertiles. Post hoc multiple
comparisons were performed using Duncan and Dunnett’s T3 for
equal and unequal variances, respectively. All nutrients and food
groups were adjusted for total energy by expressing quantities per
1000 kcal of intake. Multivariate linear regression analyses were
used to study the associations between added sugar consumption
(10 g) from solid and liquid food sources, respectively, and outcome variables of vegetables and fruit, BMI, fat mass, and waist
circumference after adjustment for age, sex, energy intake, and
physical activity. All conditions of linear regression analyses have
been met (e.g., independence, linearity, and normality). Residual
plot analysis was used as a sensitivity analysis for the regression
models. Bonferroni correction (Gelman et al. 2012) was also used
for adjusting the multiple comparisons (P < 0.004). Regression
calibration (Spiegelman et al. 1997; Hardin et al. 2003) was used to
adjust for within-person variation and potential measurement
errors by including added sugar intake on 3 individual days. All
statistical analyses were conducted using STATA version 11.0
(StataCorp LP, College Station, Tex., USA).
Results
The demographic and dietary characteristics of QUALITY participants were listed in Table 1. They consumed 51 g/day of added
sugars on average, which provided 12% of total energy intake
(204 kcal). Overall, 78% of added sugars came from solid food
sources O the top 4 sources were sweets (contributed 29% of
added sugars), baked products (25%), ready-to-eat cereal (6%), and
other snack foods (4%). The other 22% of added sugars came from
liquid sources (SSB and flavoured milk).
Compared with children in the lowest tertile of added sugars
from solid food sources (Table 2), those in the highest tertile had
statistically significantly higher intakes of total energy and percentage of energy from carbohydrate, as well as lower intakes of
% energy from protein, phosphorus, and magnesium. In addition,
higher consumption of added sugars from solid food sources was
associated with a lower intake of vegetables and fruit, lower total
HEI-C scores, and a lower percentage of participants with a good
diet. No statistically significant differences were detected for
other nutrients or for milk and dairy products.
Compared with children in the lowest tertile of added sugars
from liquid food sources (Table 3), those in the highest tertile had
significantly higher intakes of total energy and percentage of energy from carbohydrate, as well as significantly lower intakes of
percentage of energy from protein, calcium, phosphorous, magnesium, and vitamins A and D. In addition, higher consumption
of added sugars from liquid food sources was associated with
lower intakes of the 2 food groups (milk and dairy products, vegetables and fruit) and lower total HEI-C scores and a lower percentage of participants with a good diet.
837
Table 1. Dietary sources of added sugars among Quebec Adiposity and Lifestyle Investigation in Youth cohort participants at baseline (N = 613).
Mean
Basic
Age (y)
Boys (%)
BMI (kg/m2)
BMI z score
≥ BMI 85th percentile (%)
Total fat mass (kg)
Waist circumference (cm)
Physical activity (counts/min)
Diet
Total energy (kcal)
Total HEI-C score (maximum 100)
Total added sugars (g)
Solid sourcesa (g)
Sweets (g)
Baked products (g)
Ready-to-eat cereal (g)
Other snack foods (g)
Liquid sources (g)
SSB (g)
Flavoured milk (g)
SD
9.6
54.4
19.5
0.7
41.9
11.0
67.5
587
0.9
O
4.3
1.1
O
7.6
12.2
186
1675
76
51
40
15
13
2.8
2.0
11
10
1.0
391
11
25
22
14
14
4.1
3.4
12
12
2.9
Note: BMI, body mass index; HEI-C, Healthy eating index Canada (2009; Woodruff and Hanning 2010); SSB, sugarsweetened beverage.
aOnly top four solid sources of added sugars were listed.
The multivariate linear regression models (Table 4) indicate that
each additional 10 g of added sugars from solid sources was associated with a 0.3 servings/day lower of vegetables and fruit. A negative
association was detected between consumption of added sugars
from solid food sources and total fat mass, while a trend of negative
association was observed with BMI and waist circumference as well.
Consumption of each additional 10 g of added sugars from liquid
food sources was associated with 0.4 serving/day of lower vegetables
and fruit, a 0.4-kg/m2 higher BMI, a 0.5-kg greater fat mass, and a
0.9-cm higher waist circumference, respectively.
Discussion
The present study examined added sugars from both solid and
liquid food sources in a sample of Canadian children at risk of
obesity. The results suggest that higher consumption of added
sugars from either solid or liquid food sources was associated with
higher energy intake and lower overall diet quality. Higher consumption of added sugars from liquid food sources was also associated with lower intake of milk and dairy products (and related
nutrients including calcium and vitamins A and D). Positive associations with adiposity indicators were observed with consumption of added sugars from liquid food sources only.
Previous studies of added sugar have focused mainly on its liquid food sources (e.g., SSB). As solid food sources also contribute a
significant amount of added sugars (e.g., more than 60% among
Canadian youth (Langlois and Garriguet 2011)) and the lack of
studies examining the potential differences of consuming added
sugars from solid versus liquid foods, this partition of sugars was
of particular interest. To date, the only other study in youth that
examined dietary intake and its association with consuming
added sugar from different food sources reported that consumption of pre-sweetened cereals increased the likelihood of reaching
Dietary Reference Intakes for some essential shortfall micronutrients (calcium, folate, and iron), whereas consumption of SSB, candies, sweets, and sweetened grains decreased the likelihood of
meeting the recommended levels for these nutrients (Frary et al.
2004). Our study combined all solid food sources of added sugars
and found that similar to liquid sources, a higher consumption of
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838
Appl. Physiol. Nutr. Metab. Vol. 40, 2015
Table 2. Daily nutrient and food intake by tertile of added sugar from solid food sources, among Quebec Adiposity
and Lifestyle Investigation in Youth cohort participants (N = 613).
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1st tertile
Total added sugars (g)
Energy (kcal)
% Energy from protein
% Energy from fat
% Energy from carbohydrate
Calcium (mg/1000 kcal)
Phosphorus (mg/1000 kcal)
Magnesium (mg/1000 kcal)
Vitamin A (␮g/1000 kcal)
Vitamin D (␮g/1000 kcal)
Milk and dairy products (g/1000 kcal)
Vegetables and fruit (g/1000 kcal)
Total HEI-C score (maximum 100)
Good diet (≥80 score, %)
2nd tertile
3rd tertile
Mean
SD
Mean
SD
Mean
SD
P
31.8a
1437a
17.6c
32.1
51.5a
525b
673c
143b
193
3.7
178
269c
79c
50.2c
15.4
308
3.9
5.2
6.9
161
136
29
96
2.5
124
138
10
O
47.1b
1654b
15.8b
32.0
53.6b
508ab
648b
140b
197
3.7
173
243b
76b
37.2b
12.7
306
3.0
5.2
6.1
148
129
29
93
2.4
120
121
10
O
74.4c
1939c
14.3a
32.5
54.7b
492a
611a
132a
201
3.3
163
199a
73a
26.6a
24.4
378
2.4
4.4
5.6
142
121
29
80
1.9
105
106
11
O
<0.001
<0.001
<0.001
0.507
<0.001
0.077
<0.001
<0.001
0.643
0.128
0.400
<0.001
<0.001
<0.001
Note: Different lowercase letters in the same row indicate statistically significant difference among groups using ANOVA (P < 0.05) and
the letters a, b, c are marked from the lowest to the highest value. HEI-C, Healthy eating index - Canada (2009; Woodruff and Hanning 2010).
Table 3. Daily nutrient and food intake by tertile of added sugars from liquid food sources, among Quebec Adiposity
and Lifestyle Investigation in Youth cohort participants (N = 613).
1st tertile
Total added sugars (g)
Energy (kcal)
% Energy from protein
% Energy from fat
% Energy from carbohydrate
Calcium (mg/1000 kcal)
Phosphorus (mg/1000 kcal)
Magnesium (mg/1000 kcal)
Vitamin A (␮g/1000 kcal)
Vitamin D (␮g/1000 kcal)
Milk and dairy products (g/1000 kcal)
Vegetables and fruit (g/1000 kcal)
Total HEI-C score (maximum 100)
Good diet (≥80 score, %)
2nd tertile
3rd tertile
Mean
SD
Mean
SD
Mean
SD
P
38.4a
1644a
16.6b
32.3
52.5a
543b
682b
1488c
214b
3.9b
199b
266b
78b
46.9b
19.8
401
3.3
5.0
5.9
164
142
316
101
2.6
132
130
10
O
48.5b
1633a
16.2b
32.6
52.6a
504a
635a
1368b
190a
3.6ab
165a
233a
75a
33.8a
25.8
366
3.7
5.2
6.9
135
116
280
83
2.1
104
122
10
O
66.4c
1754b
14.9a
31.7
54.7b
477a
614a
1311a
187a
3.3a
148a
211a
74a
34.0a
21.7
394
3.1
4.6
6.1
145
124
255
82
2.0
105
117
11
O
<0.001
0.003
<0.001
0.232
<0.001
<0.001
<0.001
<0.001
0.004
0.023
<0.001
<0.001
<0.001
0.007
Note: Different lowercase letters in the same row indicate statistically significant difference among groups using ANOVA (P < 0.05) and
the letters a, b, c are marked from the lowest to the highest value. HEI-C, Healthy eating index - Canada (2009; Woodruff and Hanning 2010).
Table 4. Multivariate linear regression analyses of the association between added
sugars (liquid vs. solid) and vegetables and fruit and adiposity among Quebec Adiposity and Lifestyle Investigation in Youth cohort participants.
Indicators*
Vegetables and fruit (servings/d)
Solid added sugars (10 g)
Liquid added sugars (10 g)
BMI (kg/m2)
Solid added sugars (10 g)
Liquid added sugars (10 g)
Total fat mass (kg)
Solid added sugars (10 g)
Liquid added sugars (10 g)
Waist circumference (cm)
Solid added sugars (10 g)
Liquid added sugars (10 g)
N
␤ coefficient
95% CI
P
613
613
−0.28
−0.38
−0.38 to −0.18
−0.51 to −0.24
<0.001
<0.001
525
525
−0.18
0.40
−0.37 to 0.02
0.11 to 0.69
0.084
0.007
522
522
−0.39
0.52
−0.74 to −0.05
0.02 to 1.03
0.041
0.025
525
525
−0.55
0.87
−1.10 to 0.01
0.06 to 1.68
0.052
0.035
Note: BMI, body mass index; CI, confidence interval; HEI-C, Healthy eating index - Canada
(2009; Woodruff and Hanning 2010).
*Covariates included age, sex, energy intake, and physical activity.
solid added sugars was associated with a lower overall diet quality,
lower percentage of energy from protein as well as lower intake of
micronutrients and vegetables and fruit. While specific food vehicles, such as fortified breakfast cereal, may contribute positively
to overall diet, a small proportion of added sugar came from
breakfast cereals in our study. In addition, our results indicated
that those children with higher added sugar intake also consumed more energy overall but with decreased nutrient density.
In addition, our findings are consistent with previous studies
(Tordoff and Alleva 1990; Harnack et al. 1999; Rodriguez-Artalejo
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Wang et al.
et al. 2003; Vartanian et al. 2007; Libuda et al. 2009; Collison et al.
2010), showing that higher consumption of added sugar from liquid sources (mainly SSB) is linked to higher energy intake, lower
consumption of essential micronutrients, and lower overall diet
quality in youth. A cross-sectional analysis of 1112 Spanish children aged 6 to 7 years suggested that higher consumption of SSB
was associated with higher energy intake, lower consumption of
milk, calcium, and lower HEI score (Rodriguez-Artalejo et al.
2003). Another analysis of dietary data from 7156 three-day
weighed records in 1069 German youth aged 2 to 19 years found
that SSB consumption was associated with decreased micronutrient intakes (i.e., calcium and folate) as well as protein intake and
total diet quality (Libuda et al. 2009). A recent analyses of over
9400 youth aged 10 to 19 years indicated a higher intake of SSB is
associated with poor dietary choices (more fast foods and less
vegetables and fruit) (Collison et al. 2010).
Studies examining the association between consumption of
added sugars and adiposity indicators in youth remain inconclusive. Over the past 10 years, a large number of observational studies including our own findings using QUALITY data (Wang et al.
2013) report positive associations between SSB consumption and
higher risk of adiposity in both youth and adults (Malik et al.
2013). One cross-sectional analysis of nationally representative
children aged 2–18 years (n = 10 038) from the Canadian Community Health Survey 2.2 indicated that boys aged 6–11 years whose
beverage pattern characterized by soft drink had a higher prevalence of overweight and obesity (odds ratio 2.3) compared with the
lower intake group, after adjusting for various confounders. But
this beverage-weight association was not found among other age/
sex groups (Danyliw et al. 2012). Several recent studies in youth
reported negative findings with consumption of SSB or solid
added sugars (from either candy or sweets) or total added sugars.
For example, a cross-sectional analysis of 11 181 youth aged 2 to
18 years from the National Health and Nutrition Examination
Survey (NHANES) (1999–2004) found that candy consumers were
22% and 26% less likely to be overweight or obese than nonconsumers (O’Neil et al. 2011). In an analysis of 3136 youth aged 6 to
18 years from NHANES (2003–2006), Nicklas et al. (2011) reported
no significant associations between intake of total added sugars
and adiposity indicators (i.e., BMI z score, waist circumference)
with adjustment for age, sex, race, total energy intake, and physical activity. In our study, we found a cross-sectional association
between higher added sugar intake from liquid food source and
greater adiposity. Because of the cross-sectional design of this
study, the direction of the effect of the sugar–adiposity associations is not clear and it could be that some parents limit some
foods in heavier children. Added sugar from different solid
sources was combined in our study and in future studies one
might wish to examine different types of solid foods. There were a
small number of trials indicating that the sugar in liquid form
generally produces less satiety and incomplete energy compensation than sugar in solid form, and thus contributes to positive
energy balance and a higher risk of weight gain (DiMeglio and
Mattes 2000; Pan and Hu 2011). But considering the evidence of
satiety and energy intake from short-term studies is equivocal,
more randomized controlled trials of sufficient size and duration
are clearly needed to further explore the potential mechanism
between sugar intake (liquid vs. solid) and adiposity (Saris 2003;
van Baak and Astrup 2009).
The QUALITY cohort study included children at risk of obesity,
and had a sizable population of heavy children to study. The results may not be generalizable to the entire population, as youth
living in households with an obese parent may have a different
food environment, but given the current obesity rates in Canada,
this home environment of 1 obese parent is not unusual. The
recruitment from schools rather than clinics also helps to enhance the generalizability. The data for this study used measures
of three 24-h dietary recalls, several measures of adiposity (includ-
839
ing fat mass measured by DXA), and was able to control for physical activity measured by 7-day accelerometry. The food coding in
the dietary recall questionnaire enabled us to adjust for total energy intake, create food groups, and estimate added sugar values
from both solid and liquid food sources. Although it is better than
single dietary recall, this short-term recall may still limit the reliability on long-term usual intake patterns (Beaton et al. 1979). As a
global indicator to evaluate overall diet quality, the HEI-C provided advantages over other methodologies at the population
level (Kant 1996; Dubois et al. 2000), although it may be limited by
the similar weighting factor (10 points) for each component (except for “vegetables and fruit”, 20 points) (Woodruff and Hanning
2010). Canadian Nutrition File provides data on total sugars only,
without distinguishing whether it is intrinsic to the food or
added. The estimation of added sugar values was taken from the
USDA, which recently removed the Added Sugar Database from its
Web site because of constant changes in formulations for a large
number of commercial and multi-ingredient foods. Considering
there is no better added sugar database, we and others (Kell et al.
2014) chose to make use of this Added Sugar Database. Although
under-reporting is prevalent among self-reports of dietary surveys
among both older youth and adult populations (Garriguet 2008b)
and particularly “unhealthy” foods rich in fat and/or added sugars
are more frequently underestimated (Lafay et al. 2000), estimates
of under-reporting are difficult to quantify in younger children.
No specific guideline for children was made yet on the recommended consumption level of added sugars. Considering for this
potential knowledge gap for youth, our study was designed to
provide some preliminary evidence on the relationship between
added sugar consumption from solid versus liquid food sources,
diet quality, and obesity. Regarding to the potential adverse effects of consuming excessive added sugars on micronutrient dilution and health (Hess et al. 2012), the Beverage Guidance Panel
(initiated by Dr. Barry M. Popkin in the United States) has recommended limiting SSB intake for the general population in the
United States (Popkin et al. 2006). In fact, more than 30 national
and subnational governments have made efforts to restrict the
availability of SSB in schools (Hawkes 2010; Mâsse and de Niet 2013),
including voluntary actions taken by some beverage companies
(Storey 2010). Per capita intake of milk decreased from 605 to 472 mL)
per day between 1989 and 2008 in American children (Lasater et al.
2011). Although several recommendations or policies related to the
regulation of flavoured milk have been announced, no definite
agreement has been reached. Food and Nutrition Service in the
United States published Nutrition Standards for School Meals allowing schools to offer flavoured milk if it is fat-free (Food and Nutrition
Service 2014). In addition, Recommended Community Strategies published by the CDC require licensed child care facilities in local jurisdictions to ban SSB (including flavoured milk) (Khan et al. 2009), as
does the Los Angeles Unified School District Board of Education,
which has voted to remove flavoured milk from schools (Los Angeles
Unified School District 2011).
In conclusion, higher consumption of added sugars from either
solid or liquid food sources is linked to a lower diet quality in
children. Liquid, but not solid added sugars were positively associated with adiposity indicators. Further longitudinal and clinical
trial studies are encouraged, especially for examining added sugars from different solid foods, considering that there is still no
recommendation specifically for children and adolescents who
are the highest consumers of added sugar.
Conflict of interest statement
All authors reported with no conflicts of interest.
Acknowledgements
We are grateful to all the families that participated in the QUALITY
cohort. Dr. Marie Lambert (July 1952 – February 2012), pediatric
geneticist and researcher, initiated the QUALITY cohort. Her leadPublished by NRC Research Press
Appl. Physiol. Nutr. Metab. Downloaded from www.nrcresearchpress.com by Periodicals Publicacoes Tecnicas on 10/20/16
For personal use only.
840
ership and devotion to QUALITY will always be remembered and
appreciated. Dr. Jennifer O’Loughlin is a Canada Research Chair in
the early determinants of adult chronic disease. Dr. Gilles Paradis
holds an Applied Public Health Research Chair in chronic diseases
prevention. We thank Ms. Louise Johnson-Down for her technical
help in data processing and Dr. Danielle St-Arnaud-McKenzie for
her critical comments on the manuscript. Financial support:
Canadian Agri-Science Clusters Initiative, Canadian Institutes of
Health Research, Heart and Stroke Foundation of Canada, and
Fonds de la recherche en santé du Québec. All these funders had
no role in the design, analysis or writing of this article. Author
contributions: J.W.W. and K.G.-D. designed research; J.W.W. conducted research, data analyses and interpretation, and manuscript writing. L.S. contributed to the data interpretation and
critical revision; K.L. helped data entry and analyses; J.O., and G.P.
contributed on the data acquisition and interpretation and critical revision; K.G.-D. supervised the data analyses and interpretation and critical revision; J.W.W. and K.G.-D. had primary
responsibility for final content. All authors read and approved the
final version of the paper.
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