Carbohydrates, glycemic index and diabetes mellitus

No evidence of enhanced satiety following whey protein- or sucrose-enriched water beverages: a dose response trial in overweight women

Abstract

Background/Objectives:

To compare the effect of low-dose whey protein-enriched and sucrose-enriched water beverages on postprandial satiety and energy intake.

Subjects/Methods:

Sixty overweight and obese women were given water-based protein and carbohydrate (CHO) beverages or placebo on six different occasions in a double-blind, randomised cross-over study. The beverages were 2 (178 kJ) and 4% (348 kJ) protein-enriched water (Clear Protein8855), 2 (157 kJ), 4 (314 kJ) and 10% (785 kJ) sucrose-enriched water, and a sweetened water control. Beverages were matched for volume, colour, flavour and sweetness. A standardised evening meal was provided before each study day and a standardised breakfast upon arrival at the clinic at 0900 hours. The beverage preload was given midmorning at 1100 hours, and an ad libitum outcome lunch meal at 1300 hours. Subjective appetitive responses were recorded through the day until 1500 hours using visual analogue scales.

Results:

Fifty-five participants completed all six beverage conditions. Neither protein nor sucrose preloads decreased any of hunger, fullness, thoughts of food or satisfaction when compared with the sweetened water control beverage (all, P>0.05). There was also no significant effect on ad libitum energy or macronutrient intake at the outcome meal (P>0.05), with no compensation for the energy consumed within the preload beverages.

Conclusions:

There was no evidence of increased postprandial satiety or compensation for energy content at an outcome lunch meal when a water beverage was supplemented with up to 4% (w/w) whey protein or 10% (w/w) sucrose, in a group of overweight but unrestrained young and middle-aged women.

Introduction

An increasing proportion of the energy that we consume within today’s diet is in the form of beverages,1 with many individuals adding high-energy drinks into their diet throughout the day. For example, within the United States, recent data have shown that as much as 15% of daily energy intake (EI) is consumed as beverages2 where consumption of soft drinks has increased fivefold since 1950,3 and where adolescents consume almost 1.5 MJ of liquid energy per day.4 This is important since energy counts to the daily tally no matter the source, and because dietary compensation for liquids may be weaker than for solid foods with beverages being poor satiety agents.1, 5, 6, 7, 8 Although adverse effects of alcoholic beverages have been gaining gradual acceptance, not least as a consequence of adverse health effects of alcohol per se, far more controversial are the high-carbohydrate (CHO) or sugar-sweetened beverages (SSBs). A recent editorial2 has concluded that ‘calories from soft drinks do matter’ and that the time has now come to take action and implement recommendations to reduce consumption of CHO-enriched SSBs as part of a wider strategy of weight management; a finding that remains, in part, controversial9 but which is gaining considerable evidence-based support.3, 9, 10, 11

Conversely, protein-enriched beverages have received less attention. On an isoenergetic basis, higher-protein foods may enhance satiety relative to the other macronutrients12, 13, 14, 15, 16 possibly aiding weight loss,17, 18, 19, 20 and in consequence are gradually being incorporated into dietary recommendations for weight control. Protein beverages can be formulated with a wide range of composition and sensory properties, and there is a large literature of dairy protein ‘thick-shakes’ that has shown enhanced appetite control with this beverage format.21 But it is important to understand whether water-based protein-enriched beverages also enhance satiety, or whether there is poor compensation similar to that observed for SSBs. We have previously shown in a preload study that a 4% (w/w, 348kJ) protein-enriched water beverage can enhance visual analogue scale (VAS)-assessed appetite ratings relative to a zero energy water control,22 although not inducing a significant suppression of food intake despite enhanced satiety. There was some energy compensation (~70%), but the combined intake of beverage plus lunch was greater than for the zero energy control. Earlier studies have also shown enhanced appetite ratings when volume matched, isoenergetic, mixed macronutrient (protein, fat and CHO)23 or high-protein13 drinks replaced SSBs. Further, EI at an outcome meal was suppressed when high protein replaced high CHO or a low-energy control,24 protein content was titrated with CHO in a mixed nutrient beverage,25 high-protein skimmed milk replaced an isoenergetic high-CHO fruit drink,26 and in a high-protein soup study.27 However, not all beverage preload studies have reported these effects,28, 29, 30 despite these studies being of similar design, preload energy content (1–1.2 MJ) and quantity of protein administered within the beverages (20–50 g; 33–100 en% protein) compared with those studies which showed suppression of appetite13, 23 and/or EI24, 25, 26, 27 (1–1.2 MJ; 25–55 g; 17–100en% protein) versus a moderate or high-CHO beverage. A recent study has further highlighted the importance of beverage consistency and the role of sensory cues, reporting increased satiety when thick creamy protein and CHO beverages were compared with an isoenergetic water-based protein beverage.31 Whether protein composition may further differentially affect satiety32, 33 also remains poorly established.34

The aim of our current study was to compare the effect of protein- and sucrose-enriched sweetened water beverages on postprandial satiety and food intake, in a dose response study. As there is some evidence that whey may be more satiating than other dairy proteins,21, 32, 33 the water beverages were enriched with increasing doses of whey protein isolate.

Subjects and methods

Participants

Sixty healthy overweight and obese women (body mass index, BMI, 24–33 kg/m2) aged 18–45 years were recruited from the Auckland, New Zealand area by newspaper and poster advertisement, and using a consumer research recruitment company. The women were all non-smokers, with no significant health issues and no medications that may affect appetite or weight regulation. Using the Three-Factor Eating Questionnaire35 participants were confirmed as unrestrained eaters (score12 on cognitive restraint scale). Other exclusion criteria included participation in an active diet program or loss/gain of >5 kg body weight within the last 6 months. No women were pregnant or breastfeeding during the trial. All women confirmed the study foods (evening meal, breakfast and ad lib itum lunch) to be acceptable to them during pre-study screening. Participants were asked to complete questionnaires detailing their dietary behaviours on the day before each study visit. They were also given a daily diary to complete at home and menstrual cycle questionnaires at each visit to provide information on menstrual phase during the trial. Written informed consent was obtained from each participant and ethical approval was obtained from the Northern Regional Ethics Committee X, Auckland, New Zealand. The Clinical Trial registration number was ACTRN12609000723280.

Procedures

This was a double-blind, randomised, cross-over study carried out at the University of Auckland, Human Nutrition Unit (HNU). Each study day was separated by a washout period of at least 3 days, and participants were asked to refrain from consuming alcohol and/or undertaking prolonged vigorous physical activity on the day before each study day. Having consumed the standard dinner meal between 1800 hours and 2000 hours in the evening, participants arrived at the HNU appetite research facility fasted (no food or water) on the morning of each test where they were given 150 ml of water to drink before breakfast. The daily protocol is shown in Figure 1. The standardised breakfast was given at 0900 hours, which was consumed in full by participants at their own pace within 15 min. Immediately after the breakfast meal a 150 ml drink of decaffeinated black tea, coffee or water was also given. One hundred and twenty minutes after the breakfast at 1100 hours, the 500-ml test beverages were served. Beverages were served chilled, from opaque bottles and drinking glasses to minimise visual comparison, and again consumed within 15 min. A further 120 min after the test beverage at 1300 hours, an ad libitum buffet lunch meal was served where each item was provided in moderate excess and participants were instructed to eat until they felt comfortably full. Distractions were kept to a minimum on each occasion by seating participants within individual dining booths, with no reading material, laptop computers or tablets, mobile phone or other similar items. Background music was employed to dampen the sound of cutlery, crockery and the noises of eating. Participants were asked to remain in their booths for 30 min until 1330 hours, and were supervised during this time.

Figure 1
figure1

Protocol for the preload study.

Whey protein- and sucrose-enriched water beverages

Participants received each of the beverages in random order over the six visits. Beverage preloads comprised (i) water control, (ii) 2% w/w protein, (iii) 4% w/w protein, (iv) 2% w/w CHO, (v) 4% w/w CHO and (vi) 10% w/w CHO. Energy content of the preloads increased in parallel with protein and CHO content: 0% control (8 kJ), 2% (10 g protein; 178 kJ) 4% (20 g protein; 348 kJ), 2% (10 g CHO; 157 kJ) 4% (20 g CHO; 314 kJ) and 10% (50 g CHO; 785 kJ) as shown in Table 1. Glycomacropeptide content of the whey protein was low, at ~0.9% of total protein. As SSBs are known to induce poor energy compensation, a high 10% CHO preload was included in the intervention. Four percent (w/w) protein is the maximum that can be added into a clear water beverage without adverse appearance and taste effects. All preloads were matched for volume, and were sweetened and flavoured to mask the addition of up to 20 g whey protein and 50 g CHO as simple sugars. Tropical fruit colour and flavour from nature identical mango, peach and vanilla were added, plus additional masking flavour and sunset yellow colouring. The artificial sweeteners sucralose and acesulfame K were also added. The flavour of the beverages was matched as closely as possible before the study using a consumer sensory panel of 50 women (data not shown).

Table 1 Composition of the beverage preloads

Visual analogue scales

VAS were used according to the standard methodology of Blundell et al.36 The following questions were asked: ‘How hungry do you feel?/How full do you feel?/How satisfied do you feel?/How much do you think you can eat now?‘ and were anchored on the left by ‘I am not hungry/I am not full at all/I am completely empty/nothing at all‘ and ‘I am as hungry as I have ever been/I am totally full/I cannot eat another bite/a large amount‘ on the right. A set of scales rating how thirsty, energetic and relaxed the participants felt was included as a distraction from the main outcome. Ratings of nausea were also recorded. Pen and paper methods were used where participants were asked to mark their responses by placing a vertical line across a 100-mm horizontal scale. VAS measurements were collected on three occasions before the presentation of the beverages; fasted pre-breakfast (−125 min), immediately post-breakfast (−105 min) and immediately pre-treatment (−5 min). Once the beverage was given (t=0 min), VAS were recorded at 15-min intervals over the following hour (t=15, 30, 45 and 60 min), and then recorded every 30 min for the remainder of the day (t=90, 120, 150, 180, 210 and 240 min). Immediately after the standard breakfast, the beverage preloads and the outcome lunch meal participants also rated the pleasantness, visual appeal, smell, taste, aftertaste and overall palatability of each meal and/or beverage on separate 100-mm VAS (t=−105, 15 and 150 min).

Standardised meals and ad libitum lunch

Participants were provided with a standardised dinner meal on the evening before each study day and a standardised breakfast meal on the morning of the study. Evening meals were prepared at the HNU, frozen and distributed several days before the test, comprising a beef or lamb casserole with boiled rice, and a lemon dairy dessert with fruit. The energy content of the evening meal was 3.2 MJ with a fixed macronutrient composition of 24 en% fat, 29 en% protein and 47 en% CHO. Participants were asked to complete the meal by 2000 hours, to eat from the meal until they felt comfortably full, and to refrain from eating or drinking anything other than water with the meal. The standard breakfast meal was administered at the HNU and comprised toast with butter and jam or marmalade, a banana and a glass of orange juice. The energy content was 2.2 MJ with fixed macronutrient composition of 12 en% fat, 7 en% protein and 80 en% CHO.

The lunch consisted of a restricted item buffet-style meal previously shown to be appropriate for assessment of ad libitum intake.37 Food items presented were chicken or ham rice-based flan, salad leaves with standardised oil-based dressing, canned peaches, carrot and raisin loaf, and bottled water (Table 2). Before the study, it had been established with each participant that the items provided in the lunch were acceptable as meal choices. In an attempt to avoid overconsumption the variety of items presented was limited. Each meal item was provided in moderate excess and was weighed before and after the meal to determine energy and macronutrient intake, using the New Zealand-based dietary program FoodWorks (Professional Edition, Version 5, 1998-2007; Xyris Software (Australia) Pty Ltd).

Table 2 Energy and macronutrient composition of foods and beverages served at the ad libitum lunch

Statistical analyses

VAS data assessing the palatability of the four beverage conditions on a single occasion immediately after they were consumed were analysed using repeated measures Linear Mixed Model analysis of variance (ANOVA; SAS: PROC MIXED, SAS version 9.1, SAS Institute Inc, Cary, NC, USA, 2002–2003), as were VAS data assessing feelings of hunger, fullness and other satiety indicators throughout each study day. The participant, the dietary preload, the study period and the study day were included in the procedure, in addition to the beverage/time interaction that addressed whether the trajectory over time during the study period differed between conditions (beverage × time). Energy and macronutrient intake data from the ad libitum lunch meal were also analysed using repeated measures Linear Mixed Model ANOVA and included the stage of menstrual cycle in the procedure. Where the repeated measures Linear Mixed Model ANOVA was significant, Tukey’s post hoc analysis was used for pair-wise comparisons between conditions. Levene’s test for equality of variances was used to confirm equality between beverage conditions. Analyses were performed both as intention to treat (ITT) and per protocol for participants who completed all arms of the study. No differences were found and data reported are based on the per protocol analysis. Randomisation to treatment order was determined by Latin Square. No participants were replaced due to dropout after enrolment and completion of the first intervention arm. Power estimates showed 60 participants to be sufficient to detect a 10% difference in EI at the outcome lunch meal, based on a six treatment repeated measures design, and dropout of up to 15%. Missing data were assumed missing at random and no data imputation were performed. Statistical significance was set at a level of 0.05. Participant characteristics are presented as mean and standard deviation (s.d.). Efficacy end points of VAS and EI are presented as mean and standard error of the mean (s.e.m.).

Results

Participants

Sixty overweight women were randomised (Caucasian 67%, Asian 17%, Polynesian/Maori 14% and African 2%) of which 55 completed all six preload treatments. Five women withdrew from the trial following completion of at least one study visit due to inadequate time to complete the trial and/or change in work commitments. The women were overweight or obese but otherwise healthy, with a mean age of 29 years (8 s.d.) and mean BMI of 27.4 kg/m2 (2.4 s.d.). The mean restraint score of the group was 6.4 (3.9 s.d.), and all participants adhered to the inclusion criteria of a score of <12, and hence self-reported as unrestrained. Each woman was assigned to either the follicular or luteal phase of the menstrual cycle at each study visit, based on questionnaires and menstrual diary, and there was no significant difference between the phase of cycle across the six beverage conditions. Phase of menstrual cycle was not found to influence EI, or VAS-assessed appetite ratings between the six beverage conditions in this trial.

Visual analogue scales (VAS)

Palatability of the beverage preloads

The six beverages were formulated to be closely matched for appearance, palatability, flavour and sweetness. When assessed by VAS for pleasantness, visual appeal, smell, taste and palatability immediately after consumption there was no significant difference between any of the beverages (P>0.05, data not shown). There were however significant effects of aftertaste with 4% protein rated as the strongest and significantly greater than any of 2, 4 and 10% sucrose beverages (all, P<0.05). There was no significant difference between the six beverages for ratings of nausea immediately following consumption or throughout each trial day (P>0.05).

Hunger, fullness, thoughts of food and satisfaction

The mean VAS ratings for hunger, fullness, thoughts of food and satisfaction measured throughout each study day for each of the six beverage conditions are shown in Figure 2. Analyses were performed as both ITT (n=60) and completers only (n=55) groups, with no difference in outcomes between the two analysis methods. There was no significant difference in hunger, fullness, thoughts of food or satisfaction between the six beverages when analysed both during the postprandial 120 min following the preload (ANOVA, P>0.05) or throughout the full study day including the post-lunch measures (ANOVA, P>0.05), or when pair-wise comparisons were investigated.

Figure 2
figure2

Mean (s.e.m.) subjective VAS scores for hunger, fullness, satisfaction and thoughts of food for water control (), 2% w/w protein (), 4% w/w protein (□), 2% w/w CHO (Δ), 4% w/w CHO (), 10% w/w CHO () beverages. Beverage preloads were consumed at 0 min and the ad libitum lunch at 120 min.

Ad libitum lunch

Mean EI at the ad libitum lunch is presented for each beverage preload in Figure 3. There was no significant decrease in ad libitum EI when the sweetened water control was supplemented either with increasing doses of whey protein or CHO (P>0.05). Mean (s.e.m.) intake at lunch was 3008 (159) kJ following the sweetened control beverage, 2981 (164) kJ and 2913 (146) kJ following 2% and 4% protein, respectively, and 2983 (164) kJ, 3166 (155) kJ and 3088 (175) kJ following 2%, 4% and 10% CHO beverages, respectively. Relative to the control beverage, the greatest decrease in EI at lunch occurred following the 4% protein drink where there was a non-significant decrease in EI of 95 kJ (−3%, Tukey’s post hoc, P>0.05). There was no decrease in EI at lunch when the control was supplemented with the highest sucrose dose, 10% (+80 kJ,+3%, P>0.05). The 4% whey protein beverage contained an additional 348 kJ and the 10% CHO beverage contained 745 kJ. Despite the additional energy consumed midmorning in the various beverages, compensation at the lunch meal was negligible or absent (0–27%), which resulted in a higher total EI throughout the test day (breakfast+preload beverage+lunch, ANOVA, P<0.01, Table 3). All beverage treatments were higher than the water control, with pair-wise comparison showing significantly greater total EI only following the 10% CHO preload (+857 kJ, P<0.01). There was no difference in macronutrient intake for any of protein, CHO or fat eaten at the lunch meal between any of the beverage conditions (P>0.05).

Figure 3
figure3

Mean (s.e.m.) ad libitum energy intake at the lunch meal. None of the protein or sucrose beverages significantly decrease intake relative to the sweetened water control (P>0.05).

Table 3 Total energy intake throughout the study

Discussion

In this study, we found no evidence that either protein- or sucrose-enriched water beverages altered postprandial appetite scores or suppressed ad lib itum food intake from a later buffet-style lunch meal, at doses of up to 4% (w/w) protein or 10% (w/w) CHO, in a group of overweight but unrestrained young and middle-aged women. As flavoured water beverages are a commonly consumed item and whey proteins have been shown to enhance satiety,32, 33 we were interested to investigate the effects of low dose incorporation of whey proteins. The failure of the protein beverages to alter subjective appetite responses is perhaps surprising as previous studies, both by our group and other researchers, have shown changes in hunger and fullness following protein-enriched beverages,22 and some studies have even reported suppression of EI when compared with either high-sucrose or zero/low-energy control beverages.13, 16, 24, 25, 26, 27 Clearly, the sensory properties of the beverage are important as shown in the recent study by Bertenshaw et al,31 and may over-ride both macronutrient and energy content of the drink. The lack of response to the sucrose-enriched beverages in our study however is far less surprising in light of the rapidly growing evidence base for the additive energy effect of SSBs when introduced into the diet and purported adverse effects on body weight.2, 3, 9, 10, 11 Recommendations to reduce consumption of CHO-enriched SSBs as part of a wider public health strategy of weight management are gaining traction.2

Consumption of bottled waters has been rapidly increasing globally in recent years, taking up a growing proportion of the soft drinks industry. Beverages may evoke weaker appetite and compensatory responses than energy-matched solid foods,1, 6, 7, 8 although mechanisms underpinning effects of food rheology remain little explored, but achieving a low-energy water-based protein beverage that could be used as part of a higher-protein weight loss diet may be of interest to weight conscious individuals. Doses of protein above 4% w/w of course can be incorporated into thicker, shake-style protein beverages, but 4 g protein/100 g water is close to the limit of acceptance for clear water beverages. High-protein shakes have been shown to be satiety enhancing at least in part, even if not able to fully match satiety effects of higher-protein food items.24, 30 The variable findings from published protein beverage studies using preload protocols may be due to a number of reasons, including the type of protein, the dose administered and the design of these short, single day studies. Reviewing the literature provides no clear answer. Significant changes in EI have been observed following both short (for example, 30 min24, 25) and long (for example, 180 and 240 min13, 26, 27) time intervals between beverage preload and outcome meal, although short 30-min time intervals also result in no response to the preload.28, 38 Dose also does not appear to be the primary driver as lower protein studies have reported a change in EI,25, 26 whereas high-dose trials have had no effect.28, 29 Notably, we have observed different outcomes in VAS-assessed appetite responses in two well powered studies (this study, n=55; Poppitt et al.,22 n=50) using the same protein-enriched beverages, same dose, same preload protocol and same population groups. Irrespective of different VAS-assessed hunger responses, both of our studies failed to show an effect of protein up to a dose of 4% w/w (348 kJ) on later energy and macronutrient intake versus a flavour and volume matched zero energy water control22 and matched CHO beverages.

Although dietary proteins may evoke a stronger satiety response than either fats or CHOs in isoenergetic comparisons, much of the evidence has been from studies manipulating solid foods rather than liquid drinks. Whether there is a similar macronutrient hierarchy when in beverage form is not well established, although evidence of better compensation for high protein versus high CHO,13, 24, 26 and mixed macronutrient compared with sugar-only beverages23 does exist. In our current study, we did not observe a significant change in either appetite response or EI following the protein and CHO preloads relative to the water control, or when compared at matched doses. There was little or no compensation for the energy consumed within the protein drinks, as for the CHO drinks, up to the maximum tested 4% w/w protein.

Increasing the CHO dose further to a high level of 10% w/w (785 kJ) also had no effect on short-term eating behaviour, with the energy consumed within the beverage adding further to the day’s intake. The literature on SSBs and weight gain has been well reviewed in a recent article by Frank Hu.10 The review presented evidence from prospective cohort studies demonstrating a significant association between SSBs and long-term weight gain, meta-analysis of randomised controlled trials (RCT) showing decreased and increased intake of added sugars significantly decreased and increased body weight by ~1 kg, respectively, a meta-analysis of cohort studies in children showing higher intake of SSBs is associated with 55% higher risk of overweight, and RCTs also showing that decreased SSBs significantly decrease weight gain in children and adolescents.

In conclusion, there was no evidence of increased postprandial satiety or compensation for preload energy content at an ad libitum outcome lunch meal when a protein- or CHO-enriched water beverage was compared with a sweetened water control in a group of overweight but unrestrained adult women. Although there must be caution in extrapolating this finding to other age, gender or BMI cohorts, this data further add to a growing body of evidence that energy-rich beverages are likely to contribute to a positive daily energy balance and hence increase risk of weight gain.

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Acknowledgements

We thank Ramon Hall, Janie Proctor, Sofie Falk and Shelley Baty who provided technical assistance on this trial. We also thank the participants in this intervention study.

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Correspondence to S D Poppitt.

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Beverages were supplied by Fonterra Co-operative Group Ltd, New Zealand. SDP holds the Fonterra Chair in Human Nutrition at the University of Auckland, Auckland, New Zealand.

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Wiessing, K., Xin, L., Budgett, S. et al. No evidence of enhanced satiety following whey protein- or sucrose-enriched water beverages: a dose response trial in overweight women. Eur J Clin Nutr 69, 1238–1243 (2015). https://doi.org/10.1038/ejcn.2015.107

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