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European Journal of Clinical Nutrition (2004) 58, 13361341

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ORIGINAL COMMUNICATION
Effect of high levels of intense sweetener intake in
insulin dependent diabetics on the ratio of dietary
sugar to fat: a casecontrol study
M Cullen1*, J Nolan2, M Cullen2, M Moloney1,3, J Kearney4, J Lambe4 and MJ Gibney1

1
Department of Clinical Medicine, Trinity Centre for Health Sciences, Trinity College, Dublin, Ireland; 2Department of Endocrinology,
St. James Hospital, Dublin, Ireland; 3Department of Biological Sciences, Dublin Institute of Technology, Dublin, Ireland; and 4Institute
of European Food Studies, Trinity College, Dublin, Ireland

Objective: To examine the influence of intense sweetener consumption on nutrient intakes in insulin dependent diabetics
compared to controls.
Design: Case-control food consumption survey.
Setting: Dietary data were collected from individuals in Ireland between 1998 and 1999.
Subjects: Diabetics were recruited through diabetic outpatient departments of St. Jamess Hospital Dublin. Controls were friends
of the patients or staff/students of Trinity College and University College Dublin. Of the 171 diabetics contacted, 122 agreed to
participate (70% response rate) and 119 completed the study.
Interventions: In all, 3-day food diaries were used to collect the food consumption data.
Main outcome measures: Fat sugar seesaw, intense sweetness.
Results: Patients had significantly higher % energy from starch, lower % energy from sugars and a high intake of fibre compared
to controls. In both groups, there was an inverse relationship between % energy from fat and % en from sugar, with the
diabetics at the lower level of sugar intake. A score of intense sweetness intakes was computed and across tertiles of this score,
there were no significant effects on macronutrient intakes.
Conclusion: The fatsugar seesaw present in the diabetic group was at a lower level compared to the control group. A high
intake of intense sweeteners does not have a detrimental effect on macronutrient and micronutrient intakes.
Sponsorship: The Irish Universities Nutrition Alliance, a nonprofit research organisation in Trinity College, Dublin and a
postgraduate research scholarship from Enterprise Ireland (formerly Forbairt), Glasnevin, Dublin 9.
European Journal of Clinical Nutrition (2004) 58, 13361341. doi:10.1038/sj.ejcn.1601969
Published online 31 March 2004

Keywords: insulin dependent diabetics; intense sweeteners; nutrient intakes

Introduction Hinson & Nicol, 1992; Hulshof & Bouman, 1992; Bergsten,
Intense sweetener intake has been widely studied in both the 1993; CREDOC, 1994; MAFF, 1995; Toledo & Ioshi, 1995;
diabetic and general populations (Virtanen et al, 1988; Elmadfa et al, 1996; Ishiwata et al, 1998; Leclerq et al, 1999;
Heybach & Ross, 1989; MAFF, 1990; Bar & Bierman, 1992; Renwick, 1999). There is no evidence in any of these studies
that individuals exceed the Acceptable Daily Intake (ADI) of
*Correspondence: M Cullen, Food Safety Authority of Ireland, Abbey one or more intense sweeteners on a long-term basis. Indeed,
Court, Lower Abbey Street, Dublin 2, Ireland the 97.5th percentile of intakes tends to be in the order of 2
E-mail: mcullen@fsai.ie 4% of the ADI. The studies conducted by Toledo & Ioshi
Guarantor: MJ Gibney.
(1995), Heybach & Ross (1989), Renwick (1999), Virtanen
Contributors: The project was coordinated by Professor Michael
Gibney with the assistance of Dr John Kearney, Ms Mary Moloney et al (1988), MAFF (1990), Hinson & Nicol (1992) and MAFF
and Dr Joyce Lambe. Dr John Nolan and Professor Michael Cullen (1995) included diabetics in their survey groups.
provided access to their diabetic clinics and gave clinical guidance. The public health issue of intense sweetener usage is
Muireann Cullen recruited all subjects, conducted the fieldwork and
always related to the ADI, which is based on detailed
analysed the data.
Received 19 May 2003; revised 11 November 2003; accepted 3 December toxicological evaluation. However, it is possible that the
2003; published online 31 March 2004 use of intense sweeteners, displacing sugar in the diet, may
Sweetener consumption and nutrient intake
M Cullen et al
1337
lead to distortion of dietary macronutrient and micronu- Instructions on how to complete the diary were given
trient intakes. Fat and sugar, as a % of energy, have been verbally and also in written format to the subject on how
shown in several studies to be inversely related, the so-called express the quantity of foods and beverages consumed with
fat sugar seesaw (Gibney, 1990, 1995, 1998; Lewis et al, household measures or standard portions. For snacks or
1992; Maloney, 1993; Naismith et al, 1995; Flynn et al, 1996). meals purchased away from home and other foods that could
Several acute studies have been conducted to examine the not be weighed, verbal description of portions were obtained
effects of intense sweeteners on ratings of hunger and most in terms of familiar volumes, dimensions and purchasing
have found decreased or unchanged ratings of hunger units, ingredients and packaging were also described. If
(Harvey Anderson, 1995; Blackburn et al, 1997). Other acute possible, similar items were purchased by the researcher and
studies have examined the effects of intense sweetener weighed. Respondents were asked to fill in the diary after
intake on subsequent food intake and have reported either each eating occasion and to maintain their usual eating
no change (Kanders et al, 1988; Rodin, 1990; Drewnowski, habits. The diary layout enables details of every eating
1995) or a reduction in food intake (Drewnowski et al, 1994; occasion to be recorded: date, day, time, location, meal/
Rolls et al, 1988). snack, description of food or main ingredients of home-
One study has investigated the longer-term effects of made recipes, precise name (brand/flavour/type) of manu-
covert substitution of aspartame for sugar or vice versa on factured foods, cooking methods and leftovers.
patterns of nutrient intake in free-living subjects (Naismith After completing the diary, the researcher met with the
& Rhodes, 1995). In a study with free-living subjects over 10 participant to go through the previous 3 days entries,
days, covert removal of 500 kcal of sugar and its replacement checking food description, brands, ingredients of recipes,
by an equal level of aspartame led to an 8% fall in energy quantities. Queries were made to identify possible omissions
intake and an 11% rise in total fat intake. The respective such as between meal-eating occasions (beverages, confec-
covert substitution of sugar with aspartame increased energy tionery, chewing gums, snacks, etc.) or the use of tabletop
intake by 8% and decreased total fat intake by 5%. Thus, if sweeteners by inquiring after the addition of sweeteners to
the use of intense sweeteners can increase fat intake by tea, coffee, other beverages and yoghurt/desserts for the
displacing sugar, this phenomenon could also be as im- week and weekend days. The form of the sweetener (tablets/
portant as the ADI in evaluating the public health signifi- powder/liquid) and the quantity added to each bowl or cup
cance of widespread use of intense sweeteners. The present was also assessed. Participants reported the type of sweetener
study set out to examine the sugarfat relationship in a they commonly used (trade name).
group of insulin dependent diabetics who are recognized as Where necessary published average portion weights were
high users of intense sweeteners, and an age- and sex- used (Crawley, 1993). Foods were coded according to the
matched control group. McCance and Widdowson Food Composition Tables or
relevant supplements (Holland et al, 1988, 1989, 1991,
1992a, b, 1993, 1996; Chan et al, 1994, 1995, 1996). Nutrient
Methods intakes were determined using the computerized programme,
Subject selection WISP version 1.27 (Tinuvielr Software, 1998) The subjects
The protocols for this study were approved by the Joint weight (kg) and height (m) were taken following completion
Ethics Committee of St. Jamess Hospital and Federated of the diary.
Voluntary Hospitals. A total of 119 Insulin dependent Rigorous quality control of the coding and data entry
diabetics in the age range of 1675 y were recruited from procedures was performed. Each item was entered twice in
outpatients clinics of St. James Hospital. A similar number order to limit the level of error found in the database. Then a
of age (75 y) and sex-matched controls who were nondia- random 25% selection of diaries was made and these again
betic were recruited from friends of the patients or the staff were checked for inaccuracies. From this, a level of error of
and students of Trinity College Dublin and University 1% was found that being only one food code or weight/
College Dublin. portion size being incorrect in one or more of the diaries.

Dietary Survey Intense sweetener intakes


The 3-day diary used was one designed and used in the The Irish National Food Ingredient Database (Lambe, 2000)
North/South Ireland Food Consumption Survey 2000 by the was used to determine the foods on the Irish market
Irish Universities Nutrition Alliance (Harrington et al, containing intense sweeteners. This database consists of
2000a). Subjects were required to complete the diary for 2- approximately 5000 processed foods and the ingredient list
week days and 1 weekend day. Over the whole sample, the for each food. In order to find out which food contained the
beginning times for the respondents were spread out equally sweeteners of interest in this study, a search using the name
over the 7 days of the week and over seasons. Controls of the sweetener was conducted. The outcome of this search
completed the diary for the same days as their corresponding was a list of foods and their brands containing the sweetener
subjects. in question. In some cases more general groups could be

European Journal of Clinical Nutrition


Sweetener consumption and nutrient intake
M Cullen et al
1338
formed, for example, diet carbonated soft drinks. This Table 2 Mean daily intakes (with standard deviations: 7s.d.) of
resulted in a 45-item list of foods or groups of foods macronutrients and selected micronutrients in insulin dependent
diabetics and agesex-matched controls excluding the under reporters
containing intense sweeteners. in each group
Food consumption data collected from the subjects using
the 3-day diary was combined with sweetener-concentration Diabetics (n 85) Controls (n 87) P-value
data for each of the 45 foods derived from the Maximum
Permitted Levels (MPLs) given in the European Union Nutrients Mean (7s.d.) Mean (7s.d.)
Directive 34/94/EC (European Commission, 1994). This gives Energy (MJ/day) 11.173 11.473.2 0.62
intakes of intense sweeteners in mg/kg bw/day for each EI:BMR 1.670.4 1.770.4 0.18
participant in the survey.
Due to the fact that different intense sweeteners have %en fat 3676.2 35.576.2 0.58
%en pro 1673.7 14.472.8 0.002
different intensities of sweetness (International Sweeteners %en cho 43.676.9 43.878.7 0.86
Association, 2000), an index was devised for each participant %en starch 27.775.8 23.575.2 o0.001
for intense sweetness intake. This index (the Intense %en sugars 15.876.9 20.878.8 o0.001
Sweetness Intake Index) was the sum of the quotient of each %en alcohol 4.776.5 6.578.1 0.10
%en starch:sugars 2.171.2 1.477.4 o0.001
intake of an intense sweetener and the respective sweetness.
Fibre (g) 27.779.5 21.877.4 o0.0001
Calcium (mg) 1084.67421 1051.57701.1 0.71
Statistical analysis Iron (mg) 16.977.6 14.276.13 0.011
The nutrient intakes were assessed and found to be of normal Zinc (mg) 11.774.3 10.574.9 0.08
Folic acid (mg) 417.97331.5 353.47128.5 0.09
distribution. Therefore parametric tests were used in the
Vitamin C (mg) 162.37164.3 213.67200.5 0.07
analysis. The analysis conducted on both the diabetic and Vitamin D (mg) 4.672.9 3.572.2 0.003
control groups did not include under reporters (n 34 and Vitamin E (mg) 9.173.4 8.873.5 0.51
32 in diabetic and control groups, respectively). The figures Retinol (mg) 671.67547.1 546.97468.1 0.11
Carotene (mg) 2033.771586.4 2311.971498.5 0.24
presented are energy adjusted. Nutrient intakes in the
Copper (mg) 1.570.6 1.2870.4 0.006
diabetic and control groups were compared using indepen-
dent tests. The participants in each of the two groups were
divided into tertiles of % energy from fat and a two-way controls percent energy from protein (P 0.002), percent
ANOVA was used to examine the independent and inter- energy from starch (P 0.0001), percent energy from sugars
active effects of groups and tertiles. The groups were (P 0.0001), the ratio of percent energy from starch to
similarly divided into tertiles of intense sweetness intake percent energy from sugars (P 0.0001) and for the selected
index and a one-way ANOVA was conducted separately for micronutrients: fibre (P 0.0001), vitamin D (P 0.003) and
each group given the lower-range intense sweetness intake in copper (P 0.006).
the controls. These statistical analyses were carried out using The intakes of macronutrients and selected micronutrients
the SPSSs version 8.0 (SPSS Inc., 1998). for diabetics and controls, classified according to tertiles of
percent energy from total fat, are given in Table 3. Significant
differences across tertiles of percent energy from total fat
Results
were found for energy (P 0.045), percent energy from fat
The results of this study are given in Tables 14. In Table 1,
(P 0.0001), percent energy from carbohydrates
the mean values with standard deviations for age, weight,
(P 0.0001), percent energy from sugars (P 0.0001), per-
height and body mass index (BMI) for the diabetic and
cent energy from alcohol (P 0.007), ratio of percent energy
control groups are shown. Diabetics had a significantly
from starch to percent energy from sugars (P 0.007), zinc
higher (P 0.024) BMI compared to controls.
(P 0.008), vitamin E (P 0.0001), vitamin C (P 0.0001)
The mean daily nutrient intakes are given in Table 2. There
and retinol (P 0.0001). No significant interactions (group
were significant differences between the diabetics and
by tertile) were found.
In Table 4, the mean values with standard deviations are
shown for macronutrients and selected micronutrients for
Table 1 Mean values (with standard deviations: 7s.d.) for sex, age,
weight, height and body mass index (BMI) for the diabetic and control the diabetic and control groups based on tertiles of intense
subjects excluding under-reporters sweetness intake index. An ANOVA shows that there are
significant differences in the energy (mJ/day) intake in the
Diabetics (n 85) Controls (n 87) P-value diabetic tertiles only.
Mean (7s.d.) Mean (7s.d.)
Age (y) 36.5713.6 35.9714.6 0.79
Weight (kg) 74.5713.6 71.5713.3 0.15 Discussion
Height (m) 1.770.1 1.770.1 0.56 The patterns of nutrient intakes in the present study are very
BMI (kg/m2) 2674.1 24.673.6 0.02
similar to those reported for a representative sample of 1379

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Sweetener consumption and nutrient intake
M Cullen et al
1339
Table 3 Mean daily intakes (with standard deviations: s.d.) of macronutrients and selected micronutrients in insulin dependent diabetics and agesex-
matched controls based on tertiles of percent energy from fat (%enfat) excluding under reporters

Diabetic group (mean7s.d.) n 84 Control group (mean7s.d.) n 87 ANOVA

Low Medium High Low Medium High Fat tertile by


Tertiles % en fat (n 26) (n 32) (n 27) (n 27) (n 29) (n 31) Fat tertiles p group p

Energy (mJ/day) 10.474 11.472.2 12.072.5 1172.6 10.472.1 12.674.0 0.045 0.35
% Energy
Fat 28.672.7 36.271.4 42.873.6 28.272.8 35.371.4 42.073.4 o0.001 0.98
Carbohydrate 48.177.6 43.075.2 39.775.5 49.5710.5 43.576.9 39.074.7 o0.001 0.58
Protein 16.674.5 16.072.8 15.373.8 13.972.8 14.372.9 14.872.7 0.95 0.33
Starch 28.877.7 27.875.2 26.674.1 22.876.0 24.175.7 23.674.1 0.61 0.39
Sugars 19.377.4 15.376.7 13.175.2 27.6710.8 19.876.3 16.074.3 o0.001 0.15
Alcohol 7.179.5 4.875.0 2.273.0 8.5711.5 7.176.9 4.374.7 0.007 0.86
Starch:sugars 1.870.9 2.371.4 2.371 1.170.9 1.470.7 1.670.5 0.007 0.32

Fibre (g) 26.8979.8 28.979.6 27.279.1 21.178.4 21.376.8 23.077.1 0.75 0.57
Calcium (mg) 998.67377.0 1137.57441.3 1104.67438.7 992.07566.7 960.27288.2 1188.871011.2 0.46 0.479
Iron (mg) 18.0710.3 16.474.7 16.677.6 13.575.2 14.978.4 14.374.3 0.92 0.38
Zinc (mg) 11.074.5 12.074.1 12.274.4 9.274.0 9.473.3 12.7 0.008 0.34
Folic acid (mg) 486.07515.0 419.37226.2 350.77172.0 420.57146.7 318.77105.3 327.57111.4 0.019 0.79
Vitamin C (mg) 200.87197.3 154.97154.0 133.97138.1 336.97258.3 159.67134.4 156.77144.0 o0.001 0.18
Vitamin D (mg) 4.573.0 4.673.3 4.872.4 3.372.7 3.271.6 3.872.2 0.18 0.91
Vitamin E (mg) 7.672.4 8.872.5 10.974.3 7.872.8 8.372.7 10.074.4 o0.001 0.82
Retinol (mg) 545.97580.6 575.17203.6 907.27713.2 351.47168.2 455.17171.5 802.97682.6 o0.001 0.61
Carotene (mg) 1729.271395.1 2278.871805.8 2036.471484.6 2032.271249.4 2552.471754.0 2330.571444.5 0.26 0.97
Copper (mg) 1.5370.7 1.570.4 1.570.6 1.370.4 1.270.3 1.470.5 0.64 0.64

Table 4 Mean daily intakes (with standard deviations: s.d.) of macronutrients and selected micronutrients in insulin dependent diabetics and agesex-
matched controls based on tertiles of intense sweetness excluding under reporters

Diabetic group (mean7s.d.) n 84 Control group (mean7s.d.) n 87

Tertiles of intense sweetness 33.3333 0.9855 66.6666 3.0373 33.3333 0.4838 66.6666 01.7099

Nutrients Low Medium High P Low Medium High P

Energy (mJ/day) 10.372.2 10.772.0 12.573.9 0.03 11.774.0 11.372.9 11.272.6 0.69
% Energy
Fat 35.576.7 35.775.2 36.976.6 0.82 36.876.8 35.276.3 34.375.5 0.36
Carbohydrate 42.678.1 44.076.8 44.175.8 0.64 40.778.5 44.279.1 46.577.6 0.20
Protein 17.174.0 15.872.9 15.174.0 0.36 15.073.4 14.572.2 13.672.5 0.07
Starch 26.476.5 28.175.7 28.675.0 0.75 22.276.0 23.875.1 24.574.4 0.90
Sugars 16.579.2 15.975.7 15.175.2 0.93 19.3710.0 20.977.9 22.378.5 0.34
Alcohol 5.277.8 4.776.7 4.075.0 0.89 7.7711.7 6.276.1 5.775.3 0.93
Starch:sugars 2.171.1 2.171.4 2.271.0 0.97 1.671.0 1.370.6 1.370.5 0.68

Fibre (g) 24.878.2 30.3711.2 28.178.1 0.18 20.877.7 22.076.6 22.777.9 0.75
Calcium (mg) 986.67355.2 1090.47498.4 1176.57385.8 0.28 1249.371115.1 957.67285.1 947.77352.6 0.32
Iron (mg) 15.877.2 17.576.3 17.479.3 0.58 14.376.2 15.577.2 12.974.7 0.10
Zinc (mg) 12.174.3 11.074.3 12.174.3 0.56 11.776.2 10.774.6 9.173.2 0.98
Folic acid (mg) 386.07164.9 406.97239.2 461.37502.2 0.63 343.27139.8 366.57127.7 350.77120.6 0.88
Vitamin C (mg) 193.17193.1 159.07163.3 134.97131.2 0.55 157.27184.9 242.27209.4 241.27201.3 0.42
Vitamin D (mg) 4.472.6 4.773.2 4.873.0 0.83 3.472.2 3.672.3 3.372.2 0.65
Vitamin E (mg) 8.672.8 9.073.0 9.874.1 0.83 8.573.1 8.874.4 9.073 0.89
Retinol (mg) 752.17738.2 652.07552.2 611.47243.5 0.47 677.97710.1 519.27307.4 443.47211.0 0.057
Carotene (mg) 2131.671228.9 1957.071888.5 2015.271613.7 0.85 2157.771773.4 2412.871215.3 2365.271495.8 0.88
Copper (mg) 1.570.5 1.570.7 1.570.6 0.91 1.370.5 1.270.3 1.370.4 0.44

adult subjects in the North and South of Ireland (Harrington insulin dependent diabetics in the present study were very
et al, 2000b). The mean energy intakes to estimated basal close to those reported by Toeller et al (1996), in the Irish
metabolic rates (BMR) observed indicated that energy under- cohort of the multicentre EURODIAB study for similar
reporting was at an acceptable level in the present study number of diabetics including nonconsumers (n 118) with
(Goldberg et al, 1991). The pattern of nutrient intakes of the a comparable ratio of male to females subjects (65:54). In

European Journal of Clinical Nutrition


Sweetener consumption and nutrient intake
M Cullen et al
1340
both studies, the mean macronutrient intakes did not meet precision of dietary intakes for some nutrients that require
conventional goals for diabetics, indicating that more a longer recording period for accuracy.
intensive nutritional counselling of diabetics may be needed The present study was not designed to provide definitive
(Nutrition Subcommittee of the British Diabetic Association data on intense sweetener usage. Several studies have
BDA, 1991). However, the present study shows that some undertaken this task which requires very specialized meth-
areas of dietary importance to diabetics are more favourably ods, that is, receiving manufacturers information and
achieved compared to controls. Diabetics had significantly chemical analysis of the food product to ascertain the
high intakes of dietary fibre (27.7 vs 21.8 g/d), lower intakes presence of and the concentration of sweeteners. The total
of sugar (15.8 vs 20.8% energy) and higher intakes of starch intense sweetness intake index showed that the diabetics
(27.7 vs 23.5% energy). It remains to be seen whether or not had a much higher usage level of intense sweeteners in
a similar favourable pattern exists with regards to the food comparison to the controls (2.5 vs 1.4 day, P 0.0001).
consumed and this data will be presented in a future paper. ANOVA analysis was conducted within the tertiles of intense
Notwithstanding these more favourable patterns in dia- sweetness intake index for each group separately due to the
betics, the fat tertile analysis clearly shows that the fact that the tertiles were very different for each group.
frequently observed inverse relationship between fat and The direct comparison of the diets of the diabetics and
sugar as a % of energy exists both in diabetics and controls. controls across tertiles of intense sweetness intake index
This illustrated in Figure 1. The inverse relationship of sugar showed no differences in fat percent energy even though the
to fat energy exists in a similar pattern in the two groups but diabetics had double the intake of the intense sweetness
at a lower level in diabetics. The ratio of sugar to starch is also intake index. Even within groups across tertiles of intense
more favourable in the diabetic group compared to the sweetness intake index, no evidence was found in this study
controls. Based on tertiles of % en from fat, the diabetics that macronutrient intakes are significantly influenced. In
intake of sugar lowers as well as the intake of starch, whereas the diabetic group as the intense sweetness intake index
in the control, the starch intakes remain the same while the increased, the %en from sugars decreased and the %en from
sugar intakes lower. This can be expected due to the dietary starch increased but not significantly. In contrast, in the
advice the diabetics receive. Many nonsignificant results control group as the intense sweetness intake index
were found but this can be attributed to the limitation of the increased, the % en from sugars and % en from carbohy-
power of the study due to the small number of individuals drates increased. The question that arises from this study is
per tertile. A significant difference was found in the intakes whether the higher use of intense sweeteners in the control
of certain micronutrients when tertiles of %en from fat were group represents a tendency towards the consumption of
examined. Since Vitamin E is a fat-soluble vitamin, it can be foods of a sweeter nature?
expected that levels of intake would increase with increasing In conclusion, the sugarfat seesaw previously observed in
tertiles. Calcium intakes also increased probably due to a healthy subjects, is present but at a lower level in diabetics.
greater consumption of high-fat dairy products. Zinc also No evidence has been produced in the present study to show
increased as meat is a major source of this nutrient. Retinol that in a free-living population on a self-selected diet,
also increases and is found in animal foods such as fish oils intense sweetener intake influences macronutrient balance.
and liver, which suggests that a higher consumption might
occur with increasing %en from fat. Vitamin C and Folic acid
intakes decreased with increasing %en fat tertiles probably
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